The all-day pollinator visits of sunflower inflorescences in Helianthus annuus plantations are independent of head orientation: Testing a widespread hypothesis.

Mature inflorescences of sunflowers (Helianthus annuus) orient constantly on average to the geographical east. According to one of the explanations of this phenomenon, the eastward orientation of sunflower inflorescences increases the number of attracted insect pollinators. We tested this hypothesis in three field experiments performed in flowering sunflower plantations. In experiments 1 and 2 we measured the number of insects trapped by the vertical walls of sticky sunflower models facing north, east, south, and west. In experiment 3 we counted the pollinators' landings on real sunflower inflorescences facing naturally east or turned artificially toward north, south, and west. We found that the all-day number of pollinators (predominantly bees) attracted to model and real sunflowers in H. annuus plantations is independent of the azimuth direction of sunflower heads, and after 10 h in the morning, the average number of pollinators counted every 20 min is practically constant in the rest of the day.

A chromatic feature detector in the retina signals visual context changes.

The retina transforms patterns of light into visual feature representations supporting behaviour. These representations are distributed across various types of retinal ganglion cells (RGCs), whose spatial and temporal tuning properties have been studied extensively in many model organisms, including the mouse. However, it has been difficult to link the potentially nonlinear retinal transformations of natural visual inputs to specific ethological purposes. Here, we discover a nonlinear selectivity to chromatic contrast in an RGC type that allows the detection of changes in visual context. We trained a convolutional neural network (CNN) model on large-scale functional recordings of RGC responses to natural mouse movies, and then used this model to search in silico for stimuli that maximally excite distinct types of RGCs. This procedure predicted centre colour opponency in transient suppressed-by-contrast (tSbC) RGCs, a cell type whose function is being debated. We confirmed experimentally that these cells indeed responded very selectively to Green-OFF, UV-ON contrasts. This type of chromatic contrast was characteristic of transitions from ground to sky in the visual scene, as might be elicited by head or eye movements across the horizon. Because tSbC cells performed best among all RGC types at reliably detecting these transitions, we suggest a role for this RGC type in providing contextual information (i.e. sky or ground) necessary for the selection of appropriate behavioural responses to other stimuli, such as looming objects. Our work showcases how a combination of experiments with natural stimuli and computational modelling allows discovering novel types of stimulus selectivity and identifying their potential ethological relevance.

Asymmetric distribution of color-opponent response types across mouse visual cortex supports superior color vision in the sky.

Color is an important visual feature that informs behavior, and the retinal basis for color vision has been studied across various vertebrate species. While many studies have investigated how color information is processed in visual brain areas of primate species, we have limited understanding of how it is organized beyond the retina in other species, including most dichromatic mammals. In this study, we systematically characterized how color is represented in the primary visual cortex (V1) of mice. Using large-scale neuronal recordings and a luminance and color noise stimulus, we found that more than a third of neurons in mouse V1 are color-opponent in their receptive field center, while the receptive field surround predominantly captures luminance contrast. Furthermore, we found that color-opponency is especially pronounced in posterior V1 that encodes the sky, matching the statistics of natural scenes experienced by mice. Using unsupervised clustering, we demonstrate that the asymmetry in color representations across cortex can be explained by an uneven distribution of green-On/UV-Off color-opponent response types that are represented in the upper visual field. Finally, a simple model with natural scene-inspired parametric stimuli shows that green-On/UV-Off color-opponent response types may enhance the detection of 'predatory'-like dark UV-objects in noisy daylight scenes. The results from this study highlight the relevance of color processing in the mouse visual system and contribute to our understanding of how color information is organized in the visual hierarchy across species.

Highly defended nudibranchs "escape" to visually distinct background habitats.

The "escape and radiate" hypothesis predicts that once species have evolved aposematism, defended species can utilize more visually diverse visual backgrounds as they "escape" the need to be well camouflaged. This enables species to explore new ecological niches, resulting in increased diversification rates. To test this hypothesis "escape" component, we examined whether the background habitats of 12 nudibranch mollusk species differed among species depending on the presence and strength of chemical defenses. We obtained a rich array of color pattern statistics using quantitative color pattern analysis to analyze backgrounds viewed through the eyes of a potential predator (triggerfish, Rhinecanthus aculeatus). Color pattern analysis was done at viewing distances simulating an escalating predation sequence. We identified 4 latent factors comprising 17 noncorrelated color pattern parameters, which captured the among-species variability associated with differences in chemical defenses. We found that chemically defended species, indeed, were found on visually distinct backgrounds with increased color and luminance contrast, independent of viewing distance. However, we found no evidence for increased among-species background diversity coinciding with the presence and strength of chemical defenses. Our results agree with the "escape and radiate" hypothesis, suggesting that potent chemical defenses in Dorid nudibranchs coincide with spatiochromatic differences of visual background habitats perceived by potential predators.

Nanoscale ultrastructures increase the visual conspicuousness of signalling traits in obligate cleaner shrimps.

Signal theory predicts organisms should evolve signals that are conspicuous to intended receivers in natural signalling environments. Cleaner shrimps remove ectoparasites from reef fish clients and many signal their intent to clean by whipping long, white antennae. As white is a reliably conspicuous colour in aquatic environments, we hypothesized that selection has acted to increase broad-spectrum antennal reflectance in cleaners. Using scanning electron microscopy, optical models and reflectance measurements, we found that the antennae in three obligate cleaner species from two families (Palaemonidae and Lysmatidae) had thick (∼6 µm) chitinous layers or densely packed high refractive index spheres (300-400 nm diameter), which models show increase reflectance (400-700 nm). Two facultative and non-cleaning species had no visible antennae ultrastructure beyond the chitinous exoskeleton. Antennae reflectance was significantly higher in obligate cleaners than in facultative and non-cleaning species. Our results suggest that some obligate cleaners may have evolved ultrastructures that increase the conspicuousness of their antennae as signals.

Automated workflows using Quantitative Colour Pattern Analysis (QCPA): a guide to batch processing and downstream data analysis.

Animal and plant colouration presents a striking dimension of phenotypic variation, the study of which has driven general advances in ecology, evolution, and animal behaviour. Quantitative Colour Pattern Analysis (QCPA) is a dynamic framework for analysing colour patterns through the eyes of non-human observers. However, its extensive array of user-defined image processing and analysis tools means image analysis is often time-consuming. This hinders the full use of analytical power provided by QCPA and its application to large datasets. Here, we offer a robust and comprehensive batch script, allowing users to automate many QCPA workflows. We also provide a complimentary set of useful R scripts for downstream data extraction and analysis. The presented batch processing extension will empower users to further utilise the analytical power of QCPA and facilitate the development of customised semi-automated workflows. Such quantitatively scaled workflows are crucial for exploring colour pattern spaces and developing ever-richer frameworks for analysing organismal colouration accounting for visual perception in animals other than humans. These advances will, in turn, facilitate testing hypotheses on the function and evolution of vision and signals at quantitative and qualitative scales, which are otherwise computationally unfeasible. Supplementary Information: The online version contains supplementary material available at 10.1007/s10682-024-10291-7.

Allometry and ecology shape eye size evolution in spiders.

Eye size affects many aspects of visual function, but eyes are costly to grow and maintain. The allometry of eyes can provide insight into this trade-off, but this has mainly been explored in species that have two eyes of equal size. By contrast, animals possessing larger visual systems can exhibit variable eye sizes within individuals. Spiders have up to four pairs of eyes whose sizes vary dramatically, but their ontogenetic, static, and evolutionary allometry has not yet been studied in a comparative context. We report variable dynamics in eye size across 1,098 individuals in 39 species and 8 families, indicating selective pressures and constraints driving the evolution of different eye pairs and lineages. Supplementing our sampling with a recently published phylogenetically comprehensive dataset, we confirmed these findings across more than 400 species; found that ecological factors such as visual hunting, web building, and circadian activity correlate with eye diameter; and identified significant allometric shifts across spider phylogeny using an unbiased approach, many of which coincide with visual hunting strategies. The modular nature of the spider visual system provides additional degrees of freedom and is apparent in the strong correlations between maximum/minimum investment and interocular variance and three key ecological factors. Our analyses suggest an antagonistic relationship between the anterior and posterior eye pairs. These findings shed light on the relationship between spider visual systems and their diverse ecologies and how spiders exploit their modular visual systems to balance selective pressures and optical and energetic constraints.

Insights into the evolution of photoreceptor oil droplets in frogs and toads.

Photoreceptor oil droplets (ODs) are spherical organelles placed most commonly within the inner segment of the cone photoreceptors. Comprising neutral lipids, ODs can be either non-pigmented or pigmented and have been considered optically functional in various studies. Among living amphibians, ODs were only reported to occur in frogs and toads (Anura), while they are absent in salamanders and caecilians. Nonetheless, the limited understanding of their taxonomic distribution in anurans impedes a comprehensive assessment of their evolution and relationship with visual ecology. We studied the retinae of 134 anuran species, extending the knowledge of the distribution of ODs to 46 of the 58 currently recognized families, and providing a new perspective on this group that complements the available information from other vertebrates. The occurrence of ODs in anurans shows a strong phylogenetic signal, and our findings revealed that ODs evolved at least six times during the evolutionary history of the group, independently from other vertebrates. Although no evident correlation was found between OD occurrence, adult habits and diel activity, it is inferred that each independent origin involves distinct scenarios in the evolution of ODs concerning photic habits. Furthermore, our results revealed significant differences in the size of the ODs between nocturnal and arrhythmic anurans relative to the length of the cones' outer segment.

The role of collective behaviour in fish response to visual cues.

This study investigated the influence of group size (individual, groups of five, and 20) on the response of common minnow to visual cues created by vertical black and white stripes over time. The stripes were displayed on a monitor either at one end of an experimental tank, while the other was uniform white, or both ends simultaneously. Reponses were compared with a control (stripes absent). Visual cues were pseudo-randomly presented every 15-minutes over six-hours. Three predictions were made: first, due to more efficient flow of information, larger groups would respond more rapidly (Rate of response) to the visual cues. Second, assuming visual cues provide a proxy for structure and larger groups experience greater benefits of group membership due to reduced predatory risk, there will be stronger association (Strength of association and Final association) with stripes for individuals and smaller groups compared with larger groups. Consequently, the association with visual cues exhibited by larger groups would diminish over time compared to smaller, more risk averse groups. As expected, larger groups exhibited a faster Rate of response to visual cues, and individual fish a greater Strength of association compared with the largest group size. Final association, however, was more common for larger groups compared to both smaller groups and individuals. Contrary to the final prediction, responses to visual cues did not decrease over time for any group size, suggesting innate behaviour or an experimental duration insufficient to observe habituation.

Evolution of rhodopsin in flatfishes (Pleuronectiformes) is associated with depth and migratory behavior.

Visual signals are involved in many fitness-related tasks and are therefore essential for survival in many species. Aquatic organisms are ideal systems to study visual evolution, as the high diversity of spectral properties in aquatic environments generates great potential for adaptation to different light conditions. Flatfishes are an economically important group, with over 800 described species distributed globally, including halibut, flounder, sole, and turbot. The diversity of flatfish species and wide array of environments they occupy provides an excellent opportunity to understand how this variation translates to molecular adaptation of vision genes. Using models of molecular evolution, we investigated how the light environments inhabited by different flatfish lineages have shaped evolution in the rhodopsin gene, which is responsible for mediating dim-light visual transduction. We found strong evidence for positive selection in rhodopsin, and this was correlated with both migratory behavior and several fundamental aspects of habitat, including depth and freshwater/marine evolutionary transitions. We also identified several mutations that likely affect the wavelength of peak absorbance of rhodopsin, and outline how these shifts in absorbance correlate with the response to the light spectrum present in different habitats. This is the first study of rhodopsin evolution in flatfishes that considers their extensive diversity, and our results highlight how ecologically-driven molecular adaptation has occurred across this group in response to transitions to novel light environments.

Diversity and Molecular Evolution of Nonvisual Opsin Genes across Environmental, Developmental, and Morphological Adaptations in Frogs.

Nonvisual opsins are transmembrane proteins expressed in the eyes and other tissues of many animals. When paired with a light-sensitive chromophore, nonvisual opsins form photopigments involved in various nonvisual, light-detection functions including circadian rhythm regulation, light-seeking behaviors, and seasonal responses. Here, we investigate the molecular evolution of nonvisual opsin genes in anuran amphibians (frogs and toads). We test several evolutionary hypotheses including the predicted loss of nonvisual opsins due to nocturnal ancestry and potential functional differences in nonvisual opsins resulting from environmental light variation across diverse anuran ecologies. Using whole-eye transcriptomes of 81 species, combined with genomes, multitissue transcriptomes, and independently annotated genes from an additional 21 species, we identify which nonvisual opsins are present in anuran genomes and those that are also expressed in the eyes, compare selective constraint among genes, and test for potential adaptive evolution by comparing selection between discrete ecological classes. At the genomic level, we recovered all 18 ancestral vertebrate nonvisual opsins, indicating that anurans demonstrate the lowest documented amount of opsin gene loss among ancestrally nocturnal tetrapods. We consistently found expression of 14 nonvisual opsins in anuran eyes and detected positive selection in a subset of these genes. We also found shifts in selective constraint acting on nonvisual opsins in frogs with differing activity periods, habitats, distributions, life histories, and pupil shapes, which may reflect functional adaptation. Although many nonvisual opsins remain poorly understood, these findings provide insight into the diversity and evolution of these genes across anurans, filling an important gap in our understanding of vertebrate opsins and setting the stage for future research on their functional evolution across taxa.

Wavelength-specific negatively phototactic responses of the burrowing mayfly larvae Ephoron virgo.

Mayflies are typically negatively phototactic during larval development, whereas the adults possess positive phototaxis. However, no extensive research has been done into the wavelength dependence of phototaxis in any mayfly larvae. We measured the repellency rate of Ephoron virgo larvae to light as a function of wavelength in the 368-743 nm spectral range. We established that the magnitude of repellence increased with decreasing wavelength and the maximal responses were elicited by 400 nm violet light. This wavelength dependence of phototaxis is similar to the recently reported spectral sensitivity of positive phototaxis of the twilight-swarming E. virgo adults. Negative phototaxis not only facilitates predation evasion: avoidance of the blue-violet spectral range could also promote the larvae to withdraw towards the river midline in the case of a drop in the water level, when the underwater light becomes enriched with shorter wavelengths as a result of the decreasing depth of overhead river water.

Localization of multiple opsins in ocular and non-ocular tissues of deep-sea shrimps and the first evidence of co-localization in a rhabdomeric R8 cell (Caridea: Oplophoroidea).

Bioluminescence is a prevalent phenomenon throughout the marine realm and is often the dominant source of light in mesophotic and aphotic depth horizons. Shrimp belonging to the superfamily Oplophoroidea are mesopelagic, perform diel vertical migration, and secrete a bright burst of bioluminescent mucous when threatened. Species in the family Oplophoridae also possess cuticular light-emitting photophores presumably for camouflage via counter-illumination. Many species within the superfamily express a single visual pigment in the retina, consistent with most other large-bodied mesopelagic crustaceans studied to date. Photophore-bearing species have an expanded visual opsin repertoire and dual-sensitivity visual systems, as evidenced by transcriptomes and electroretinograms. In this study, we used immunohistochemistry to describe opsin protein localization in the retinas of four species of Oplophoroidea and non-ocular tissues of Janicella spinicauda. Our results show that Acanthephyra purpurea (Acanthephyridae) retinas possess LWS-only photoreceptors, consistent with the singular peak sensitivity previously reported. Oplophoridae retinas contain two opsin clades (LWS and MWS) consistent with dual-sensitivity. Oplophorus gracilirostris and Systellaspis debilis have LWS in the proximal rhabdom (R1-7 cells) and MWS2 localized in the distal rhabdom (R8 cell). Surprisingly, Janicella spinicauda has LWS in the proximal rhabdom (R1-7) and co-localized MWS1 and MWS2 opsin paralogs in the distal rhabdom, providing the first evidence of co-localization of opsins in a crustacean rhabdomeric R8 cell. Furthermore, opsins were found in multiple non-ocular tissues of J. spinicauda, including nerve, tendon, and photophore. These combined data demonstrate evolutionary novelty and opsin duplication within Oplophoridae, with implications for visual ecology, evolution in mesophotic environments, and a mechanistic understanding of adaptive counter-illumination using photophore bioluminescence.

A Review of Cervidae Visual Ecology.

This review examines the visual systems of cervids in relation to their ability to meet their ecological needs and how their visual systems are specialized for particular tasks. Cervidae encompasses a diverse group of mammals that serve as important ecological drivers within their ecosystems. Despite evidence of highly specialized visual systems, a large portion of cervid research ignores or fails to consider the realities of cervid vision as it relates to their ecology. Failure to account for an animal's visual ecology during research can lead to unintentional biases and uninformed conclusions regarding the decision making and behaviors for a species or population. Our review addresses core behaviors and their interrelationship with cervid visual characteristics. Historically, the study of cervid visual characteristics has been restricted to specific areas of inquiry such as color vision and contains limited integration into broader ecological and behavioral research. The purpose of our review is to bridge these gaps by offering a comprehensive review of cervid visual ecology that emphasizes the interplay between the visual adaptations of cervids and their interactions with habitats and other species. Ultimately, a better understanding of cervid visual ecology allows researchers to gain deeper insights into their behavior and ecology, providing critical information for conservation and management efforts.

Red vision in animals is broadly associated with lighting environment but not types of visual task.

Red sensitivity is the exception rather than the norm in most animal groups. Among species with red sensitivity, there is substantial variation in the peak wavelength sensitivity (λmax) of the long wavelength sensitive (LWS) photoreceptor. It is unclear whether this variation can be explained by visual tuning to the light environment or to visual tasks such as signalling or foraging. Here, we examine long wavelength sensitivity across a broad range of taxa showing diversity in LWS photoreceptor λmax: insects, crustaceans, arachnids, amphibians, reptiles, fish, sharks and rays. We collated a list of 161 species with physiological evidence for a photoreceptor sensitive to red wavelengths (i.e. λmax ≥ 550 nm) and for each species documented abiotic and biotic factors that may be associated with peak sensitivity of the LWS photoreceptor. We found evidence supporting visual tuning to the light environment: terrestrial species had longer λmax than aquatic species, and of these, species from turbid shallow waters had longer λmax than those from clear or deep waters. Of the terrestrial species, diurnal species had longer λmax than nocturnal species, but we did not detect any differences across terrestrial habitats (closed, intermediate or open). We found no association with proxies for visual tasks such as having red morphological features or utilising flowers or coral reefs. These results support the emerging consensus that, in general, visual systems are broadly adapted to the lighting environment and diverse visual tasks. Links between visual systems and specific visual tasks are commonly reported, but these likely vary among species and do not lead to general patterns across species.

Backgrounds and the evolution of visual signals.

Color signals which mediate behavioral interactions across taxa and contexts are often thought of as color 'patches' - parts of an animal that appear colorful compared to other parts of that animal. Color patches, however, cannot be considered in isolation because how a color is perceived depends on its visual background. This is of special relevance to the function and evolution of signals because backgrounds give rise to a fundamental tradeoff between color signal detectability and discriminability: as its contrast with the background increases, a color patch becomes more detectable, but discriminating variation in that color becomes more difficult. Thus, the signal function of color patches can only be fully understood by considering patch and background together as an integrated whole.

Ecological and morphological correlates of visual acuity in birds.

Birds use their visual systems for important tasks, such as foraging and predator detection, that require them to resolve an image. However, visual acuity (the ability to perceive spatial detail) varies by two orders of magnitude across birds. Prior studies indicate that eye size and aspects of a species' ecology may drive variation in acuity, but these studies have been restricted to small numbers of species. We used a literature review to gather data on acuity measured either behaviorally or anatomically for 94 species from 38 families. We then examined how acuity varies in relation to (1) eye size, (2) habitat spatial complexity, (3) habitat light level, (4) diet composition, (5) prey mobility and (6) foraging mode. A phylogenetically controlled model including all of the above factors as predictors indicated that eye size and foraging mode are significant predictors of acuity. Examining each ecological variable in turn revealed that acuity is higher in species whose diet comprises vertebrates or scavenged food and whose foraging modes require resolving prey from farther away. Additionally, species that live in spatially complex, vegetative habitats have lower acuity than expected for their eye sizes. Together, our results suggest that the need to detect important objects from far away - such as predators for species that live in open habitats, and food items for species that forage on vertebrate and scavenged prey - has likely been a key driver of higher acuity in some species, helping us to elucidate how visual capabilities may be adapted to an animal's visual needs.

How Oratosquilla oratoria compound eye response to the polarization of light: In the perspective of vision genes and related proteins.

The special rhabdom structure of the mid-band ommatidium in compound eye contributes to the mantis shrimp being the only animal species known to science that can recognize circularly polarized light (CPL). Although the number of mid-band ommatidium of Oratosquilla oratoria is reduced, the mid-band ommatidium still has orthogonal geometric interleaved rhabdom and short oval distal rhabdom, which may mean that the O. oratoria has weakened circular polarized light vision (CPLV). Here we explored the molecular mechanisms of how O. oratoria response to the polarization of light. Based on the specific expression patterns of vision-related functional genes and proteins, we suggest that the order of light response by O. oratoria compound eye was first natural light, then left-circularly polarized light (LCPL), linearly polarized light, right-circularly polarized light (RCPL) and dark. Meanwhile, we found that the expression levels of vision-related functional genes and proteins in O. oratoria compound eye under RCPL were not significantly different from those in DL, which may imply that O. oratoria cannot respond to RCPL. Furthermore, the response of LCPL is likely facilitated by the differential expression of opsin and microvilli - related functional genes and proteins (arrestin and sodium-coupled neutral amino acid transporter). In conclusion, this study systematically illustrated for the first time how O. oratoria compound eye response to the polarization of light at the genetic level, and it can improve the visual ecological theory behind polarized light vision evolution.

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies.

The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arises across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-million-year-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. Using a combination of selection analyses on visual opsin sequences, in vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy and neural tracing, we quantify and describe physiological, anatomical and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including: (i) relaxed selection on visual opsins, perhaps mediated by habitat preference, (ii) interspecific shifts in visual system physiology and anatomy, and (iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at the perceptual, processing and molecular level.

Measures and models of visual acuity in epipelagic and mesopelagic teleosts and elasmobranchs.

Eyes in low-light environments typically must balance sensitivity and spatial resolution. Vertebrate eyes with large "pixels" (e.g., retinal ganglion cells with inputs from many photoreceptors) will be sensitive but provide coarse vision. Small pixels can render finer detail, but each pixel will gather less light, and thus have poor signal relative-to-noise, leading to lower contrast sensitivity. This balance is particularly critical in oceanic species at mesopelagic depths (200-1000 m) because they experience low light and live in a medium that significantly attenuates contrast. Depending on the spatial frequency and inherent contrast of a pattern being viewed, the viewer's pupil size and temporal resolution, and the ambient light level and water clarity, a visual acuity exists that maximizes the distance at which the pattern can be discerned. We develop a model that predicts this acuity for common conditions in the open ocean, and compare it to visual acuity in marine teleost fishes and elasmobranchs found at various depths in productive and oligotrophic waters. Visual acuity in epipelagic and upper mesopelagic species aligned well with model predictions, but species at lower mesopelagic depths (> 600 m) had far higher measured acuities than predicted. This is consistent with the prediction that animals found at lower mesopelagic depths operate in a visual world consisting primarily of bioluminescent point sources, where high visual acuity helps localize targets of this kind. Overall, the results suggest that visual acuity in oceanic fish and elasmobranchs is under depth-dependent selection for detecting either extended patterns or point sources.