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Animal colour patterns are a model system for understanding evolution because they are unusually accessible for study and experimental manipulation. This is possible because their functions are readily identifiable. In this final paper of the symposium we provide a diagram of the processes affecting colour patterns and use this to summarize their functions and put the other papers in a broad context. This allows us to identify significant ‘holes’ in the field that only become obvious when we see the processes affecting colour patterns, and their interactions, as a whole. We make suggestions about new directions of research that will enhance our understanding of both the evolution of colour patterns and visual signalling but also illuminate how the evolution of multiple interacting traits works. This article is part of the themed issue ‘Animal coloration: production, perception, function and application’.

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion-vine butterfly Heliconius erato by using color- and pattern-manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.

Animal coloration patterns, from zebra stripes to bird egg speckles, are remarkably varied. With research on the perception, function, and evolution of animal patterns growing rapidly, we require a convenient framework for quantifying their diversity, particularly in the contexts of camouflage, mimicry, mate choice, and individual recognition. Ideally, patterns should be defined by their locations in a low-dimensional pattern space that represents their appearance to their natural receivers, much as color is represented by color spaces. This synthesis explores the extent to which animal patterns, like colors, can be described by a few perceptual dimensions in a pattern space. We begin by reviewing biological spatial vision, focusing on early stages during which neurons act as spatial filters or detect simple features such as edges. We show how two methods from computational vision—spatial filtering and feature detection—offer qualitatively distinct measures of animal coloration patterns. Spatial filters provide a measure of the image statistics, captured by the spatial frequency power spectrum. Image statistics give a robust but incomplete representation of the appearance of patterns, whereas feature detectors are essential for sensing and recognizing physical objects, such as distinctive markings and animal bodies. Finally, we discuss how pattern space analyses can lead to new insights into signal design and macroevolution of animal phenotypes. Overall, pattern spaces open up new possibilities for exploring how receiver vision may shape the evolution of animal pattern signals.

The ability to identify and retain logical relations between stimuli and apply them to novel stimuli is known as relational concept learning. This has been demonstrated in a few animal species after extensive reinforcement training, and it reveals the brain's ability to deal with abstract properties. Here we describe relational concept learning in newborn ducklings without reinforced training. Newly hatched domesticated mallards that were briefly exposed to a pair of objects that were either the same or different in shape or color later preferred to follow pairs of new objects exhibiting the imprinted relation. Thus, even in a seemingly rigid and very rapid form of learning such as filial imprinting, the brain operates with abstract conceptual reasoning, a faculty often assumed to be reserved to highly intelligent organisms.

Evidenced in zebrafishes skin and Mimulus petal, Turing-like mechanisms are probably responsible for many periodic color patterns of Eukaryotes. They are characterized by the mathematical relationships linking their cellular or molecular actors, the periodicity and the geometrical range of the patterns they produce: spots, stripes or mazes. Nevertheless, some periodic patterns such as leopard iconic rosettes required additional ingredients to explain their formation. Growth being the main candidate, we extensively explore its multiple facets, at the Eukaryotes scale. We show that far beyond the particular feline coat pattern, putative-growth Turing color patterns are present in many diverse lineages of plants and animals and seem absent in Fungi and unicellular lineages. Using models, we show the many ways growth can induce new shapes and colors, and that putative-growth pattern locations correlates with tissue hot spots of growth, suggesting the latter as the underlying mechanism. By reverse reasoning, we show that growth effects could reveal crucial information about pattern formation. We show how putative growth patterns can contribute to influence organisms visibility, thereby improving camouflage or aposematism. Our results demonstrate the range of morphogenetic roles that tissue expansion can take, by interacting with a scale-sensitive mechanism, here Turing-like patterning. Considering this extensive overview of its biological importance, both qualitatively and quantitatively, links between growth and form might more than ever needed to be explored.

Animals with color vision use color information in intra- and interspecific communication, which in turn may drive the evolution of conspicuous colored body traits via natural and sexual selection. A recent study found that the transparent wings of small flies and wasps in lower-reflectance light environments display vivid and stable structural color patterns, called “wing interference patterns” (WIPs). Such WIPs were hypothesized to function in sexual selection among small insects with wing displays, but this has not been experimentally verified. Here, to our knowledge we present the first experimental evidence that WIPs in males of Drosophila melanogaster are targets of mate choice from females, and that two different color traits—saturation and hue—experience directional and stabilizing sexual selection, respectively. Using isogenic lines from the D. melanogaster Genetic Reference Panel, we compare attractiveness of different male WIPs against black and white visual backgrounds. We show that males with more vivid wings are more attractive to females than are males with dull wings. Wings with a large magenta area (i.e., intermediate trait values) were also preferred over those with a large blue or yellow area. These experimental results add a visual element to the Drosophila mating array, integrating sexual selection with elements of genetics and evo-devo, potentially applicable to a wide array of small insects with hyaline wings. Our results further underscore that the mode of sexual selection on such visual signals can differ profoundly between different color components, in this case hue and saturation. Significance Recently, it was discovered that small insects like flies and wasps, with seemingly transparent wings, display vivid coloration against dark backgrounds because of so-called “wing interference patterns” (WIPs). It was proposed that such wing coloration could function in sexual selection and species recognition, but direct evidence for this hypothesis has been lacking. Here, to our knowledge we present the first experimental evidence that WIPs in male Drosophila melanogaster are targets of mate choice from females. Comparison of attractiveness of different male WIPs between black and white backgrounds revealed that two different color traits, saturation and hue, experience directional and stabilizing sexual selection, respectively. Our results suggest that vivid coloration in WIPs is a target of mate choice and might have evolved by sexual selection.

Color pattern plays a crucial role in various aspects of an organism’s biology, including camouflage, mating, and communication. Despite its significance, methods to quantify and study color pattern variation are often lacking, especially for complex patterns that defy simple categorization. In this study, we developed algorithms to capture and obtain data on 19 different pattern measurements from digital images of 55 individuals of the Eastern box turtle Terrapene carolina sampled in the field and in a museum. The Eastern box turtle is an ideal species to study variation of complex color patterns as this species is easily encountered in the field and in museum collections in Northeastern US, has a relatively easy to identify bright color pattern against a dark background, and has a rigid shell structure, which removes problems related to body distortion. The selected measurements capture the different aspects of the complexity of the color pattern, including the symmetry of the pattern on the turtles’ scutes, a critical component in developmental and evolutionary studies. We estimated the variation of each of these 19 measurements across our samples. We determined how much of this variation was influenced by the sensitivity of the pattern capture algorithm due to non-standardized elements of the image acquisition, lighting conditions, and animal shape on pattern variation. To our knowledge, this is the first study to use a comprehensive set of pattern measurements to capture variation in a complex color pattern while also assessing the susceptibility of each of these measurements to noise introduced during data collection. Additionally, we carried out a citizen science approach to characterize the complexity of the color pattern based on human perception and determine which of the 19 pattern measurements best describe this complexity. The most variable measurements across individuals were blue and yellow contrast between the pattern and non-pattern coloration and the average size of objects. From our estimates of the measurement noise due to image acquisition and analysis, we found that the contrast differences reflected true pattern variations between individual turtles, whereas differences in the average size of objects were influenced by both individual turtle variation and measurement inconsistencies. We found that due to the complexity of the patterns, measurements had lower variability if they did not depend on the algorithm defining a set of discrete objects. For example, total area had much less measurement variability than average object area. Our study provides a comprehensive workflow and tools to study variation in complex color patterns in organisms sampled under non-standardized conditions while also estimating the influence of noise due to biological and non-biological factors.

During metamorphosis, the wings of a butterfly sprout hundreds of thousands of scales with intricate microstructures and nanostructures that determine the wings’ optical appearance, wetting characteristics, thermodynamic properties, and aerodynamic behavior. Although the functional characteristics of scales are well known and prove desirable in various applications, the dynamic processes and temporal coordination required to sculpt the scales’ many structural features remain poorly understood. Current knowledge of scale growth is primarily gained from ex vivo studies of fixed scale cells at discrete time points; to fully understand scale formation, it is critical to characterize the time-dependent morphological changes throughout their development. Here, we report the continuous, in vivo, label-free imaging of growing scale cells of Vanessa cardui using speckle-correlation reflection phase microscopy. By capturing time-resolved volumetric tissue data together with nanoscale surface height information, we establish a morphological timeline of wing scale formation and gain quantitative insights into the underlying processes involved in scale cell patterning and growth. We identify early differences in the patterning of cover and ground scales on the young wing and quantify geometrical parameters of growing scale features, which suggest that surface growth is critical to structure formation. Our quantitative, time-resolved in vivo imaging of butterfly scale development provides the foundation for decoding the processes and biomechanical principles involved in the formation of functional structures in biological materials.

Flowering patterns are crucial to understand the dynamics of plant reproduction and resource availability for pollinators. Seasonal climate constrains flower and leaf phenology, where leaf and flower colors likely differ between seasons. Color is the main floral trait attracting pollinators; however, seasonal changes in the leaf-background coloration affect the perception of flower color contrasts by pollinators. For a seasonally dry woody cerrado community (Brazilian savanna) mainly pollinated by bees, we verified whether seasonality affects flower color diversity over time and if flower color contrasts of bee-pollinated species differ between seasons due to changes in the leaf-background coloration. For 140 species, we classified flower colors based on human-color vision, and for 99 species, we classified flower colors based on bee-color vision (spectral measurements). We described the community’s flowering pattern according to the flower colors using a unique 11 years phenological database. For the 43 bee-pollinated species in which reflectance data were also available, we compared flower color diversity and contrasts against the background between seasons, considering the background coloration of each season. Flowering was markedly seasonal, peaking at the end of the dry season (September), when the highest diversity of flower colors was observed. Yellow flowers were observed all year round, whereas white flowers were seasonal, peaking during the dry season, and pink flowers predominated in the wet season, peaking in March. Bee-bluegreen flowers peaked between September and October. Flowers from the wet and dry seasons were similarly conspicuous against their corresponding background. Regardless of flowering season, the yellowish background of the dry season promoted higher flower color contrast for all flower species, whereas the greener background of the wet season promoted a higher green contrast. Temporal patterns of flower colors and color contrasts were related to the cerrado seasonality, but also to bee’s activity, visual system, and behavior. Background coloration affected flower contrasts, favoring flower conspicuousness to bees according to the season. Thus, our results provide new insights regarding the temporal patterns of plant–pollinator interactions.

Vivid structural colours in butterflies are caused by photonic nanostructures scattering light. Structural colours evolved for numerous biological signalling functions and have important technological applications. Optically, such structures are well understood, however insight into their development in vivo remains scarce. We show that actin is intimately involved in structural colour formation in butterfly wing scales. Using comparisons between iridescent (structurally coloured) and non-iridescent scales in adult and developing H. sara , we show that iridescent scales have more densely packed actin bundles leading to an increased density of reflective ridges. Super-resolution microscopy across three distantly related butterfly species reveals that actin is repeatedly re-arranged during scale development and crucially when the optical nanostructures are forming. Furthermore, actin perturbation experiments at these later developmental stages resulted in near total loss of structural colour in H. sara . Overall, this shows that actin plays a vital and direct templating role during structural colour formation in butterfly scales, providing ridge patterning mechanisms that are likely universal across lepidoptera. NCOMMS-23-44446C Vivid structural colours in butterflies are caused by photonic nanostructures scattering light, however insight into the development of such structures in vivo remains scarce. Here the authors show that actin plays a vital and direct templating role during structural colour formation in butterfly scales, providing ridge patterning mechanisms that are likely universal across lepidoptera.