Activation of butterfly eyespots by Distal-less is consistent with a reaction-diffusion process.
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ABSTRACT:
SUBMITTER: Connahs H
PROVIDER: S-EPMC6526720 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundThe border ocellus, or eyespot, is a conspicuous color pattern element in butterfly wings. For two decades, it has been hypothesized that transcription factors such as Distal-less (Dll) are responsible for eyespot pattern development in butterfly wings, based on their expression in the prospective eyespots. In particular, it has been suggested that Dll is a determinant for eyespot size. However, functional evidence for this hypothesis has remained incomplete, due to technical difficulties.ResultsHere, we show that ectopically expressed Dll induces ectopic elemental color patterns in the adult wings of the blue pansy butterfly, Junonia orithya (Lepidoptera, Nymphalidae). Using baculovirus-mediated gene transfer, we misexpressed Dll protein fused with green fluorescent protein (GFP) in pupal wings, resulting in ectopic color patterns, but not the formation of intact eyespots. Induced changes included clusters of black and orange scales (a basic feature of eyespot patterns), black and gray scales, and inhibition of cover scale development. In contrast, ectopic expression of GFP alone did not induce any color pattern changes using the same baculovirus-mediated gene transfer system.ConclusionsThese results suggest that Dll plays an instructive role in the development of color pattern elements in butterfly wings, although Dll alone may not be sufficient to induce a complete eyespot. This study thus experimentally supports the hypothesis of Dll function in eyespot development.
| S-EPMC4774158 | biostudies-literature
Project description:Unsolved problemThe development of eyespots on the wing surface of butterflies of the family Nympalidae is one of the most studied examples of biological pattern formation.However, little is known about the mechanism that determines the number and precise locations of eyespots on the wing. Eyespots develop around signaling centers, called foci, that are located equidistant from wing veins along the midline of a wing cell (an area bounded by veins). A fundamental question that remains unsolved is, why a certain wing cell develops an eyespot, while other wing cells do not.Key idea and modelWe illustrate that the key to understanding focus point selection may be in the venation system of the wing disc. Our main hypothesis is that changes in morphogen concentration along the proximal boundary veins of wing cells govern focus point selection. Based on previous studies, we focus on a spatially two-dimensional reaction-diffusion system model posed in the interior of each wing cell that describes the formation of focus points. Using finite element based numerical simulations, we demonstrate that variation in the proximal boundary condition is sufficient to robustly select whether an eyespot focus point forms in otherwise identical wing cells. We also illustrate that this behavior is robust to small perturbations in the parameters and geometry and moderate levels of noise. Hence, we suggest that an anterior-posterior pattern of morphogen concentration along the proximal vein may be the main determinant of the distribution of focus points on the wing surface. In order to complete our model, we propose a two stage reaction-diffusion system model, in which an one-dimensional surface reaction-diffusion system, posed on the proximal vein, generates the morphogen concentrations that act as non-homogeneous Dirichlet (i.e., fixed) boundary conditions for the two-dimensional reaction-diffusion model posed in the wing cells. The two-stage model appears capable of generating focus point distributions observed in nature.ResultWe therefore conclude that changes in the proximal boundary conditions are sufficient to explain the empirically observed distribution of eyespot focus points on the entire wing surface. The model predicts, subject to experimental verification, that the source strength of the activator at the proximal boundary should be lower in wing cells in which focus points form than in those that lack focus points. The model suggests that the number and locations of eyespot foci on the wing disc could be largely controlled by two kinds of gradients along two different directions, that is, the first one is the gradient in spatially varying parameters such as the reaction rate along the anterior-posterior direction on the proximal boundary of the wing cells, and the second one is the gradient in source values of the activator along the veins in the proximal-distal direction of the wing cell.
| S-EPMC4633216 | biostudies-literature
Project description:Plasticity is often regarded as a derived adaptation to help organisms survive in variable but predictable environments, however, we currently lack a rigorous, mechanistic examination of how plasticity evolves in a large comparative framework. Here, we show that phenotypic plasticity in eyespot size in response to environmental temperature observed in Bicyclus anynana satyrid butterflies is a complex derived adaptation of this lineage. By reconstructing the evolution of known physiological and molecular components of eyespot size plasticity in a comparative framework, we showed that 20E titer plasticity in response to temperature is a pre-adaptation shared by all butterfly species examined, whereas expression of EcR in eyespot centers, and eyespot sensitivity to 20E, are both derived traits found only in a subset of species with eyespots.
| S-EPMC7012602 | biostudies-literature
Project description:Development can bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely. The eyespots commonly found on butterfly wings each have concentric rings of differing colors, and these serially repeated pattern elements have been a focus for evo-devo research. In the butterfly family Nymphalidae, eyespots have been shown to function in startling or deflecting predators and to be involved in sexual selection. Previous work on a model species of Mycalesina butterfly, Bicyclus anynana, has provided insights into the developmental control of the size and color composition of individual eyespots. Experimental evolution has also shown that the relative size of a pair of eyespots on the same wing surface is highly flexible, whereas they are resistant to diverging in color composition, presumably due to the underlying shared developmental process. This fixed color composition has been considered as a prime example of developmental bias with significant consequences for wing pattern evolution. Here, we test this proposal by surveying eyespots across the whole subtribe of Mycalesina butterflies and demonstrate that developmental bias shapes evolutionary diversification except in the genus Heteropsis which has gained independent control of eyespot color composition. Experimental manipulations of pupal wings reveal that the bias has been released through a novel regional response of the wing tissue to a conserved patterning signal. Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus, allowing rapid morphological change, facilitating evolutionary diversification.
| S-EPMC7959562 | biostudies-literature
Project description:Research has shown that the mere presence of stimuli that resemble eyes is sufficient to attract attention, elicit aesthetic responses, and can even enhance prosocial behavior. However, it is less clear whether eye-like stimuli could also be used as a tool for nature conservation. Several animal species, including butterflies, develop eye-like markings that are known as eyespots. In the present research, we explored whether the mere display of eyespots on butterfly wings can enhance: (a) liking for a butterfly species, and (b) attitudes and behaviors towards conservation of a butterfly species. Four online experimental studies, involving 613 participants, demonstrated that eyespots significantly increased liking for a butterfly species. Furthermore, eyespots significantly increased positive attitudes towards conservation of a butterfly species (Studies 1, 2 and 4), whereas liking mediated the eyespot effect on conservation attitudes (Study 2). However, we also found some mixed evidence for an association between eyespots and actual conservation behavior (Studies 3 and 4). Overall, these findings suggest that eyespots may increase liking for an animal and sensitize humans to conservation. We discuss possible implications for biodiversity conservation and future research directions.
| S-EPMC4636354 | biostudies-literature
Project description:Large conspicuous eyespots on butterfly wings have been shown to deter predators. This has been traditionally explained by mimicry of vertebrate eyes, but recently the classic eye-mimicry hypothesis has been challenged. It is proposed that the conspicuousness of the eyespot, not mimicry, is what causes aversion due to sensory biases, neophobia or sensory overloads. We conducted an experiment to directly test whether the eye-mimicry or the conspicuousness hypothesis better explain eyespot efficacy. We used great tits (Parus major) as model predator, and tested their reaction towards animated images on a computer display. Birds were tested against images of butterflies without eyespots, with natural-looking eyespots, and manipulated spots with the same contrast but reduced resemblance to an eye, as well as images of predators (owls) with and without eyes. We found that mimetic eyespots were as effective as true eyes of owls and more efficient in eliciting an aversive response than modified, less mimetic but equally contrasting eyespots. We conclude that the eye-mimicry hypothesis explains our results better than the conspicuousness hypothesis and is thus likely to be an important mechanism behind the evolution of butterfly eyespots.
| S-EPMC4426626 | biostudies-other
Project description:Complex behaviour in many systems arises from the stochastic interactions of spatially distributed particles or agents. Stochastic reaction-diffusion processes are widely used to model such behaviour in disciplines ranging from biology to the social sciences, yet they are notoriously difficult to simulate and calibrate to observational data. Here we use ideas from statistical physics and machine learning to provide a solution to the inverse problem of learning a stochastic reaction-diffusion process from data. Our solution relies on a non-trivial connection between stochastic reaction-diffusion processes and spatio-temporal Cox processes, a well-studied class of models from computational statistics. This connection leads to an efficient and flexible algorithm for parameter inference and model selection. Our approach shows excellent accuracy on numeric and real data examples from systems biology and epidemiology. Our work provides both insights into spatio-temporal stochastic systems, and a practical solution to a long-standing problem in computational modelling.
| S-EPMC4894951 | biostudies-literature
Project description:Understanding how novel complex traits originate involves investigating the time of origin of the trait, as well as the origin of its underlying gene regulatory network in a broad comparative phylogenetic framework. The eyespot of nymphalid butterflies has served as an example of a novel complex trait, as multiple genes are expressed during eyespot development. Yet the origins of eyespots remain unknown. Using a dataset of more than 400 images of butterflies with a known phylogeny and gene expression data for five eyespot-associated genes from over twenty species, we tested origin hypotheses for both eyespots and eyespot-associated genes. We show that eyespots evolved once within the family Nymphalidae, approximately 90 million years ago, concurrent with expression of at least three genes associated with early eyespot development. We also show multiple losses of expression of most genes from this early three-gene cluster, without corresponding losses of eyespots. We propose that complex traits, such as eyespots, may have originated via co-option of a large pre-existing complex gene regulatory network that was subsequently streamlined of genes not required to fulfill its novel developmental function.
| S-EPMC3420954 | biostudies-literature
Project description:Vertebrate and invertebrate colour pattern determination mechanisms are considered distinct; recently, however, both fish and butterfly colour patterns have been partly explained by reaction-diffusion mechanisms. Here, we show that multi-coloured eyespots of the spotted mandarin fish, which are reminiscent of butterfly eyespots, are determined by the serial induction of colour patterns. The morphological characterisation of eyespots indicates a sequence of colour pattern development and dynamic interactions between eyespots. A substantial part of an eyespot can be surgically removed and is then reconstructed by regeneration. Strikingly, ectopic patterns are induced by damage at a background (eyespotless) area, but focal damage did not change the eyespot size. Early stages of damage repair were accompanied by calcium oscillations. These results demonstrate that fish eyespots are determined by serial induction, which is likely based on a reaction-diffusion mechanism. These findings suggest mechanistic similarities between the fish and butterfly systems.
| S-EPMC3289039 | biostudies-other
Project description:Shapes and patterns observed in internal organs and tissues are reproducibly and robustly produced over a long distance (up to millimeters in length). The most fundamental remaining question is how these long geometries of shape and pattern form arise from the genetic message. Recent studies have demonstrated that extracellular matrix (ECM) critically participates as a structural foundation on which cells can organize and communicate. ECMs may be a key to understanding the underlying mechanisms of long-distance patterning and morphogenesis. However, previous studies in this field mainly focused on the complexes and interaction of cells and ECM. This paper pays particular attention to ECM and demonstrates that collagen, a major ECM component, natively possesses the reproducible and definite patterning ability reaching centimeter-scale length. The macroscopic pattern consists of striped transparent layers. The observation under crossed Nicols demonstrates that the layers consist of alternately arranged polarized and unpolarized parts. Confocal fluorescence microscopy studies revealed that the polarized and unpolarized segments include collagen-rich and -poor regions, respectively. The patterning process was proposed based on the Liesegang banding formation, which are mineral precipitation bands formed in hydrogel matrixes. These findings will give hints to the questions about long-distance cell alignment and provide new clues to artificially control cell placement over micron size in the field of regenerative medicine.
| S-EPMC8756805 | biostudies-literature