Evolutionary Ecology

Batesian mimics, such as hoverflies, can gain protection by resembling noxious species that predators avoid, such as bees. Such resemblance can be behavioural as well as morphological. Bees commonly have a preference for blue flowers, whilst flies generally prefer yellow and white. We predicted that, driven by selection for enhanced mimicry, bee-mimicking hoverflies would have switched flower preference from yellow to blue, to follow the flower choices of their models. We gathered internet photographs of flower-visiting bees and wasps, their hoverfly mimics, and non-mimicking hoverflies, and compared the colours of the visited flowers. Flowers visited by bumblebees were "bluer" than those visited by other hymenopterans (honeybees, wasps and solitary bees). Correspondingly, flowers visited by bumblebee-mimicking hoverflies were bluer than those visited by non-mimics, and were indistinguishable in blueness from those visited by bumblebees. There was no such pattern in flower "yellowness", where all flies and most hymenopterans preferred similar yellowness, and only bumblebees chose less yellow flowers than the others. Our study demonstrates widespread changes in microhabitat choice (specifically flower preference) among a diverse group of Batesian mimics, consistent with the idea of behavioural mimicry. Mildly noxious models such as bumblebees are thought to exert particularly strong selection for mimetic accuracy, suggesting that habitat-choice mimicry may be selected as a way of enhancing morphological mimicry.

The evolution of visual traits in closely-related species living in sympatry is highly influenced by their ecological interactions: while sexual selection tends to promote the divergence of visual cues involved in mate choice, natural selection via predation may promote the convergence of dissuasive signals between prey species, especially in unpalatable or evasive prey. Here, we investigate the impact of sympatry on the evolution of the blue structural colouration in the wings of two closely-related Morpho butterfly species across several localities throughout Central and South America. Dorsal iridescence might affect mate choice and species recognition, which should promote its local divergence among species. However, the bright flashes and dynamic colour patterns produced by iridescence during flight might also increase survival by confusing predators and favouring escape. Such an effect might in turn lead to convergence in wing iridescence between evasive species occurring in sympatry, a phenomenon dubbed evasive mimicry. To test the effect of these putative antagonistic selective forces on visual cues evolution, we quantified the variation of the structural blue colour displayed at 13 different combinations of illumination/observation angles, on the wings of two closely-related Morpho species. We contrasted 10 sympatric and 11 allopatric locations and specifically compared the phenotypic distances between individuals from different species. Phenotypic distances between heterospecific pairs of individuals were significantly smaller in sympatry, consistent with the hypothesis of a local convergence of iridescence due to evasive mimicry. Interestingly, sexual dimorphism was found between males and females, suggesting that the trade-off between natural and sexual selection on the evolution of iridescence might differ between sexes. Our results suggest that local predation pressures may promote repeated evolutionary convergence of structural colouration between evasive prey species living in sympatry.

Herbivory degree and the ratio of generalist to specialist herbivores have long been treated as two important but independent factors in shaping the evolution of plant defense. However, this assumption of independency is poorly supported and has resulted in great controversy in explaining the patterns of plant defense. Here we investigated the possible interaction between herbivory degree and generalist-to-specialist ratio using a cost-benefit model of defense evolution in plants. Our results showed that, with increasing generalist herbivore proportion, plant defense investment increases when herbivory degree is low and decreases when herbivory degree is high. These results provide the first theoretical support for the interactive effect of herbivory degree and ratio of generalist/specialist affecting plant defense, which integrate many of the previous results (e.g. latitudinal patterns of plant defense and defense evolution of invasive plants) and put them into a more general theoretical context.

Visual camouflage evolves within the bounds of lights interaction with the surroundings and the sensory limits of its observers. Rapid temporal variation in lighting from weather and its interaction with objects within the visual scene alters the contrast of the spatio-chromatic features of both backgrounds and animals, the latter through self-shading and received shadows from their surroundings. Despite the apparent effect of lighting on object appearance, the enormity of interactions and the diversity of animal phenotypic solutions present challenges to investigating the combined effects of lighting and habitat structure on camouflage effectiveness and design. Genetic algorithms and mathematical animal pattern generation provide a potential solution to investigating this high-dimensional feature space. Here, an online artificial evolution experiment was used to examine the effect of lighting and habitat geometry on camouflage. Lighting and geometry changed which prey phenotypes evolved, and the predictive power of common camouflage metrics. Crucially, lighting condition systematically altered prey-targets internal contrast and interacted with habitat geometry, affecting the evolved patterning, colour, and countershading. Our work demonstrates the importance of considering the relative geometry and lighting of an environment when determining the function of animal colouration and the adaptive value of camouflage.

Transparency reduces prey detectability by predators. While transparent aquatic species hold higher transparency levels as the light availability of their habitat increases, less is known about such variation in terrestrial species. Lepidoptera species exhibiting transparent wings display various levels of transparency. Using two complementary approaches, we explore how the evolution of different transparency degrees relates to habitat openness, activity rhythm and mimicry syndrome (bee/wasp versus dead-leaf mimic). First, by exposing artificial moth-like prey to wild avian predators in a range of habitat openness, we show that survival is lower in more open habitats. We also found that less transparent morphs are more attacked than more transparent ones, regardless of habitat openness degree. Second, by analysing the evolution of wing features and ecological traits in 107 clearwing species, we found that diurnal species transmit more light than nocturnal species under certain conditions (when considering only forewings, at smaller clearwing surfaces and at larger wing lengths) and that species flying in open habitats and exhibiting large percentages of clearwing surface transmit slightly more light than those flying in closed habitats, although this is reversed at smaller percentages of clearwing surfaces. Additionally, bee/wasp mimics are more often diurnal and have higher and less variable light transmittances than dead-leaf mimics, which are more often nocturnal. Flying during the day, in open habitats and mimicking insects with transparent wings seem to promote high light transmittance under certain circumstances. Activity rhythm, habitat openness and species interactions play a crucial role in determining transparency design on land.

The evolution of ecological specialization can be summed up in a single question: why would a species evolve a more-restricted niche space? Various hypotheses have been developed to explain the promotion or suppression of ecological specialization. One hypothesis, competitive diversification, states that increased intraspecific competition will cause a population to broaden its niche breadth. With individuals alike in resource use preference, more individuals reduce the availability of preferred resources and should grant higher fitness to those that use secondary resources. However, recent studies cast doubt on this hypothesis with increased intraspecific competition reducing niche breadth in some systems. We present a game-theoretic evolutionary model showing greater ecological specialization with intraspecific competition under specific conditions. This is in contrast to the competitive diversification hypothesis. Our analysis reveals that specialization can offer a competitive advantage. Largely, when facing weak competition, more specialized individuals are able to acquire more of the preferred resources without greatly sacrificing secondary resources and therefore gain higher fitness. Only when competition is too great for an individual to significantly affect resource use will intraspecific competition lead to an increased niche breadth. Other conditions, such as a low diversity of resources and a low penalty to specialization, help promote ecological specialization in the face of intraspecific competition. Through this work, we have been able to discover a previously unseen role that intraspecific competition plays in the evolution of ecological specialization.

AbstractCoevolution between two species can lead to exaggerated phenotypes that vary in a cor-related manner across space. However, the conditions under which we expect such spatially varying coevolutionary patterns in polygenic traits are not well-understood. We investigate the coevolutionary dynamics between two species undergoing reciprocal adaptation across space and time, using simulations inspired by the Taricha newt - Thamnophis garter snake system. One striking observation from this system is that newts in some areas carry much more tetrodotoxin than in other areas, and garter snakes that live near more toxic newts tend to be more resistant to this toxin, a correlation seen across several broad geographic areas. Furthermore, snakes seem to be "winning" the coevolutionary arms race, i.e., having a high level of resistance compared to local newt toxicity, despite substantial variation in both toxicity and resistance across the range. We explore how possible genetic architectures of the toxin and resistance traits would affect the coevolutionary dynamics by manipulating both mutation rate and effect size of mutations across many simulations. We find that coevolutionary dynamics alone were not sufficient in our sim-ulations to produce the striking mosaic of levels of toxicity and resistance observed in nature, but simulations with ecological heterogeneity (in trait costliness or interaction rate) did produce such patterns. We also find that in simulations, newts tend to "win" across most combinations of genetic architectures, although the species with higher mutational genetic variance tends to have an advantage.

Forests are a mosaic of light spectra, and colour signal efficiency might change in different light environments. Local adaptation in Heliconius butterflies is linked to microhabitat use and the colourful wing colour patterns may be adapted for signalling in different light environments. These toxic butterflies exhibit conspicuous colours as a warning to predators that they should be avoided, but also find and choose potential mates based on colour signals. The two selection pressures of predation and mate preference are therefore acting together. Colour conspicuousness should show habitat-specific contrast for the butterflies, which would facilitate detection and species identification. On the other hand, selection for signal stability would be stronger in the avian visual system. In this study we analysed the contrast of two Heliconius mimicry rings in their natural habitats under varying degrees of forest fragmentation and light conditions. We used digital image analyses and mapped the bird and butterfly vision colour space in order to examine whether warning colours have greater contrast and if they transmit a consistent signal across time of the day and habitat in a tropical forest. We tested conspicuousness using opponent colour channels against a natural green background. For avian vision, colours are generally very stable through time and habitat. For butterfly vision, there is some evidence that species are more contrasting in their own habitats, where conspicuousness is higher for red and yellow bands in the border and for white in the forest. Light environment affects Heliconius butterflies warning signal transmission to a higher degree through their own vision, but to a lesser degree through avian predator vision. This work provides insight into the use of colour signals in sexual and natural selection in the light of ecological adaptation.

Pollen participates both as the carrier of male gametes in the reproduction of flowering plants and as a key resource exploited by floral visitors, especially bees. Pollinator behavior significantly alters the patterns of pollen removal and deposition, often called pollen fates. To date, few theoretical investigations have attempted to jointly model patterns of pollen transfer and pollinator behavior, and empirical studies are restricted to species to which pollen movement can be tracked. Here we use a spatially explicit agent-based modeling approach, to determine how bee grooming behavior may alter pollen fates and affect plant reproduction. Specifically, we asked whether pollen mixing and removal during pollen grooming may change the "pollen landscape" on a bees body consequently affecting both pollen export by the anthers and deposition onto stigmas. Our model shows that both mixing and removal behaviors restructure the "pollen landscape" on the bees body, increasing pollen carryover (deposition in consecutive visits), and increasing pollen diversity (number of pollen donors) onto stigmas in sequential flower visits. Our results counterintuitively show that pollen grooming may have a positive effect on both male and female finesses during plant reproduction.

Predator-prey systems often feature periodic population cycles. In an empirical system with a heritable prey defence trait, ecological oscillations were previously shown to cause evolution of prey defence on the timescale of the population cycles. In this paper, we develop an eco-evolutionary mathematical model comprising partial differential equations to investigate the evolutionary dynamics of prey defence during population cycles. We reveal that ecological population cycles induce evolutionary oscillations of the mean prey defence trait. In contrast to existing continuum modelling frameworks, our model allows for the evolution of individual variability. We show that eco-evolutionary oscillations select for increased individual variability close to the transition from stable to oscillatory states. We also reveal that evolution of prey defence requires both high efficiency and low cost of prey defence and highlight that more information on trade-offs between cost and efficiency is required.

Using a dynamic optimisation model for juvenile fish in stochastic food environments, we investigate optimal hormonal regulation, energy allocation and foraging behaviour of a growing host infected by a parasite that only incurs an energetic cost. We find it optimal for the infected host to have higher levels of orexin, growth- and thyroid hormones, resulting in higher activity levels, increased foraging, and faster growth. This growth strategy thus displays several of the fingerprints often associated with parasite manipulation: higher levels of metabolic hormones, faster growth, higher allocation to reserves (i.e. parasite-induced gigantism), higher risk taking and eventually higher predation rate. However, there is no route for manipulation in our model, so these changes reflect adaptive host compensatory responses. Interestingly, several of these changes also increase the fitness of the parasite. Our results call for caution when interpreting observations of gigantism or risky host behaviours as parasite manipulation without further testing.

Mating cues are often comprised of several elements, which can act independently, or in concert to attract a suitable partner. Individual elements may also function in other contexts, such as anti-predator defense or camouflage. In Heliconius butterflies, wing patterns comprise several individual color pattern elements, which advertise the butterflies toxicity to predators. These wing patterns are also mating cues, and males predominantly court females that possess the same wing pattern as their own. However, it is not known whether male preference is based on the full wing pattern or only individual pattern elements. We compared preferences of male H. erato lativitta between female models with the full wing pattern and those with some pattern elements removed. We found no differences in preference between the full wing pattern model and a model with pattern elements removed, indicating that the complete composition of all elements is not essential to the mating signal. Wing pattern preferences also contribute to pre-mating isolation between two other Heliconius taxa, H. erato cyrbia and H. himera, therefore, we next compared preferences for the same models in these species. H. erato cyrbia and H. himera strongly differed in preferences for the models, potentially providing a mechanism for how pre-mating isolation acts between these species. These findings suggest that contrasting levels of selective constraint act on elements across the wing pattern.

Butterflies often show adaptive phenotypic plasticity where environmental cues during early stages are used to produce a phenotype that maximizes fitness in the environment experienced by adults. Many tropical satyrine butterflies (Nymphalidae: Satyrinae) are seasonally polyphenic and produce distinct wet- and dry-season form adults providing tight environment-phenotype matching in seasonal environments. Dry-season forms, which are expressed in the dry season, can be induced in the laboratory by growing larvae at low temperatures or on poor food quality. Since both these factors also tend to reduce larval growth rate, larval growth rate may be an internal cue that translates the environmental cues into the expression of phenotypes. If this is the case, we predict that slower-growing larvae would be more likely to develop a dry-season phenotype. To test this hypothesis, we measured both larval growth rate and adult phenotype (eyespot size and wing shape) of individuals of the common evening brown butterfly (Melanitis leda), reared at various temperatures and on various host-plant species. We found that among treatments, larvae with lower growth rates (low temperature, particular host plants) were more likely to develop dry-season phenotypes (small eyespots, falcate wing tips), but within treatments, larval growth rate was mainly linked to wing shape, not eyespot size. These relationships tended to be stronger for males than females as males showed a wider range of eyespot sizes and wing shapes. Overall, only plasticity in wing shape appears to be (partly) mediated by larval growth, and in a sex-specific manner.

Understanding environmental and ecological effects on ecosystem structure, function, and dynamics is crucial. However, our comprehension of such effects remains challenging due to the complex interplay of abiotic environment, ecological relationships among species, and coevolution within and across trophic levels. Here, we set out to investigate a wide range of combined ecoevolutionary responses in a plant-insect ecosystem. We study ecological population dynamics, coevolution and functional diversity in response to changes in (1) abiotic-biotic interactions, (2) within-trophic-level competitive interactions, and (3) between-trophic-level antagonistic and mutualistic interactions. We developed an eco-evolutionary and functional trait-based model to simulate environmental and ecologically mediated responses to these interactions. We show that mutualistic interactions render a positive feedback loop of increased population sizes followed by selection for even stronger biotic ecological interactions instead of abiotic interactions. Antagonistic interactions have the opposite effect and adaptation to abiotic environment becomes more important. Furthermore, our study reveals that benign conditions (high ecological opportunities, low within-trophic-level competition, and strong interactions between plants and insects) facilitate functional diversity, whereas harsh conditions impede diversity. These findings provide valuable insights into mechanisms that underlie fundamental eco-evolutionary responses to current environmental and ecological changes, offering potential contributions to ecosystem conservation facing urgent challenges.

The outcome of evolution sometimes appears to be predictable, as in the evolution of the same characteristics independently in convergent evolution. Other times, evolutions path depends on starting conditions or chance events, and some forms evolve just once and never appear again. Is convergence, and by implication, predictability, a common characteristic of the evolutionary process? We aimed to answer this question by using an evolutionary video game titled Project Hastur as a study system. In this video game, the enemies evolve traits to help them combat the players strategy. We determined whether the same environmental pressures (in this case, player strategy) lead to predictable evolution. We conducted a series of experiments with three different playing styles and four different evolutionary treatments with varying kinds of selection pressure, each with several replicates. For each replicate, enemies from the first and final generations were categorized into types using k-means clustering. The Euclidean distance between the cluster centroids and the sum of squares values were recorded for each replicate and compared among evolutionary treatments using Wilcoxon rank sum tests. Evolutionary predictability was evaluated using permutation tests. We found that fitness functions in Project Hastur led to incredible, but unpredictable, diversity. The fitness landscape changes between replicates, even within the same experimental treatment and regardless of player strategy, resulting in enemies with an unpredictable array of trait values.

O_LIUnderstanding how environmental change is shaping organismal morphology of key functional guilds is important, since morphological traits determine the delivery of ecosystem services we depend upon. Adult butterflies, as pollinators, are commercially and culturally important, but the longitudinal data across appropriate time frames to understand trait response trends are generally limited. C_LIO_LIHere we leverage digitised museum butterfly specimens to help fill this data gap by employing automated methods (machine learning and Elliptical Fourier Analysis) to achieve high-throughput measurements of traits across large collections. We analyse how wing shape (the outline of the whole butterfly) varies in over 178,000 specimens of 65 butterfly species collected across the UK and Ireland over two centuries. C_LIO_LIWe identify two major biologically attributable axes of butterfly wing shape: aspect ratio and asymmetry. Analysing a subset of these specimens (108,511 from 34 species), we find directional trends in wing shape. Over a period of 105 years (1901-2006), wings generally became narrower and longer in over half (18) of the studied species. This response may be affecting butterfly behaviour by favouring gliding flight. C_LIO_LIUltimately, we highlight that historical processes including temperature change have historically shaped butterfly wing shape. We demonstrate that studying whole wing outline using automated methods allows us to extract the high-throughput, long-term data required to understand the responses of ecologically important taxa at scales that we were previously unable to achieve. C_LI

Lepidoptera - a group of insects in which wing transparency has arisen multiple times - exhibit much variation in the size and position of transparent wing zones. However, little is known as to how this variability affects detectability. Here, we test how the size and position of transparent elements affect predation of artificial moths by wild birds in the field. We also test whether deep neural networks (DNNs) might be a reasonable proxy for live predators, as this would enable one to rapidly test a larger range of hypotheses than is possible with live animals. We compare our field results with results from six different DNN architectures (AlexNet, VGG-16, VGG-19, ResNet-18, SqueezeNet, and GoogLeNet). Our field experiment demonstrated the effectiveness of transparent elements touching wing borders at reducing detectability, but showed no effect of transparent element size. DNN simulations only partly matched field results, as larger transparent elements were also harder for DNNs to detect. The lack of consistency between wild predators and DNNs responses raises questions about what both experiments were effectively testing, what is perceived by each predator type, and whether DNNs can be considered to be effective models for testing hypotheses about animal perception and cognition.

Islands serve as natural laboratories for exploring evolutionary processes, often fostering unique species through their isolation and distinct ecological conditions. These environments present opportunities to study how a range of selective pressures shape biodiversity. Bird plumage colouration is one trait that has shown to consistently change in island populations, and predation has been hypothesized to influence these differences. While animals often face a trade-off between signalling to conspecifics and avoiding detection by predators, the role of predation in shaping conspicuousness remains underexplored experimentally. In this study, we asked how predation pressure differs between insular and mainland habitats, and whether predation risk covaries with conspicuousness of male and female birds across environments. In a field experiment, we investigated predation rates using 3D-printed models painted to represent both sexes of 12 bird species from three archipelagos (Madeira, Azores, and Canary Islands) and their closest mainland relatives. These models were deployed in the species natural environments to measure hit rates (a proxy for predation risk), accounting for factors that influence prey detectability, such as colour of the models, background contrast, and vegetation. We found that models on the islands experienced less hits compared to those on the mainland, while sexual dichromatic models were more likely to be dislodged on the mainland. In addition, for mainland sites, increased chromatic contrast correlated with a higher probability of dislodgment, suggesting that more conspicuous models were more likely to be hit. These results highlight that while predation constrains conspicuousness, other ecological and evolutionary factors likely drive the reduced plumage colouration observed in island birds. Our research offers experimental insights into how predation interacts with conspicuous traits in shaping plumage colouration in birds.

Camouflage and warning signals are contrasted prey strategies reducing predator attack, which offer an excellent opportunity to study the evolutionary forces acting on prey appearance. Edible prey are often inconspicuous and escape predation by remaining undetected. Predators learn to find the most common ones, leading to apostatic selection (advantage to rare morphs) enhancing variation in cryptic prey. By contrast, defended prey are often conspicuous and escape predation by using warning colorations identifying them as unprofitable. Predators avoid the ones they are most familiar with, leading to positive frequency-dependence and warning signal uniformity. It is less clear, however, what happens when two morphs of the same species vary strongly in conspicuousness, and how to explain the maintenance of cryptic and conspicuous morphs within populations, in the case of profitable prey. Using the white and melanic morphs of the invasive Box Tree Moth (Cydalima perspectalis) presented at three different frequencies, we investigate whether a) caterpillars and adult moths are palatable for birds, b) the less conspicuous, melanic morph experiences lower predation rates and b) whether frequency-dependence balances morph frequencies. Our results suggest that the melanic morph enjoys a survival advantage owing to a lower visibility. However, our experiments show that, unexpectedly, the two color morphs experience opposite patterns of frequency-dependent predation, despite being both fully palatable to birds. The melanic morph is under apostatic selection, whereas the conspicuous, white morph is subject to positive frequency-dependence (safety in numbers). Our experiments also show some level of unpalatability in the caterpillars. These results offer novel insight into how predation triggers contrasting evolutionary patterns in a palatable, polymorphic species within two morphs that differ markedly in conspicuousness and within two different life stages. Lay summaryUnderstanding the factors influencing character variation in natural populations is a key question in evolutionary ecology. Predation is one of the main drivers of color evolution in prey communities and prey usually mitigate predation using camouflage or warning colors. Camouflage evolves because it lowers the probability of being detected by predators. Since predators are more efficient at finding prey which they are familiar with, prey which display a rare phenotype are favoured (negative frequency-dependent selection). By contrast, aposematism is defined by conspicuous appearance in toxic or otherwise unprofitable prey, and evolves because birds identify defended prey by learning to use their appearance as a warning signal. The most common signals are usually best identified and avoided (positive-frequency dependent selection). It is not clear, however, how these two forces combine when predators are facing cryptic and conspicuous morphs of the same species, and how to explain their coexistence. Here we investigate this question in a laboratory experiment, by presenting wild birds with a melanic and a white morph of the same moth. Unexpectedly, our results show that despite being both fully palatable to birds, the two color morphs are subject to very different types of selection depending on their frequencies. The melanic morph is favored when it is rare, the conspicuous white morph as it gets common. The simultaneous action of these forces may contribute to maintain color polymorphism in natural populations. We also show that caterpillars of this species are unpalatable and chemically defended, whereas adults are not, showing opposite strategies of predator defense in different life stages of the same species.

Conspicuous colors have fascinated biologists for centuries, leading to much research on the evolution and functional significance of color traits. However, some authors have critiqued the adaptationist dogma amongst color researchers. When investigating a color trait, researchers often exclusively consider the alternative hypotheses--they assume color is adaptive. The null hypothesis of animal color--that coloration is non-adaptive or evolutionary neutral, is rarely considered. Here, we use phylogenetic comparative methods to investigate color evolution throughout freshwater crayfishes. Within the taxa we analyzed, conspicuous colors have evolved independently over 50 times. The intuitive, but not evolutionary-justified assumption when presented these results is to assume that these colors are an adaptation. But contrary to this intuition, our work might support the hypothesis that coloration in crayfish is neutral; because we show that conspicuous colors are evolutionary correlated to a semi-terrestrial burrowing lifestyle. Conspicuous coloration being common in semi-terrestrial burrowers is paradoxical, because these species are nocturnal, and rarely leave their burrows. Overall, our work brings into question to traditional view of animal coloration as a perfectly adapted phenotype.