Evolution and spectral tuning of visual pigments in birds and mammals

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.     

Flexible responses to visual and olfactory stimuli by foraging Manduca sexta: larval nutrition affects adult behaviour

Here, we show that the consequences of deficient micronutrient (β-carotene) intake during larval stages of Manduca sexta are carried across metamorphosis, affecting adult behaviour. Our manipulation of larval diet allowed us to examine how developmental plasticity impacts the interplay between visual and olfactory inputs on adult foraging behaviour. Larvae of M. sexta were reared on natural (Nicotiana tabacum) and artificial laboratory diets containing different concentrations of β-carotene (standard diet, low β-carotene, high β-carotene and cornmeal). This vitamin-A precursor has been shown to be crucial for photoreception sensitivity in the retina of M. sexta. After completing development, post-metamorphosis, starved adults were presented with artificial feeders that could be either scented or unscented. Regardless of their larval diet, adult moths fed with relatively high probabilities on scented feeders. When feeders were unscented, moths reared on tobacco were more responsive than moths reared on β-carotene-deficient artificial diets. Strikingly, moths reared on artificial diets supplemented with increasing amounts of β-carotene (low β and high β) showed increasing probabilities of response to scentless feeders. We discuss these results in relationship to the use of complex, multi-modal sensory information by foraging animals.     

Defining the V5/MT neuronal pool for perceptual decisions in a visual stereo-motion task

In the primate visual cortex, neurons signal differences in the appearance of objects with high precision. However, not all activated neurons contribute directly to perception. We defined the perceptual pool in extrastriate visual area V5/MT for a stereo-motion task, based on trial-by-trial co-variation between perceptual decisions and neuronal firing (choice probability (CP)). Macaque monkeys were trained to discriminate the direction of rotation of a cylinder, using the binocular depth between the moving dots that form its front and rear surfaces. We manipulated the activity of single neurons trial-to-trial by introducing task-irrelevant stimulus changes: dot motion in cylinders was aligned with neuronal preference on only half the trials, so that neurons were strongly activated with high firing rates on some trials and considerably less activated on others. We show that single neurons maintain high neurometric sensitivity for binocular depth in the face of substantial changes in firing rate. CP was correlated with neurometric sensitivity, not level of activation. In contrast, for individual neurons, the correlation between perceptual choice and neuronal activity may be fundamentally different when responding to different stimulus versions. Therefore, neuronal pools supporting sensory discrimination must be structured flexibly and independently for each stimulus configuration to be discriminated.This article is part of the themed issue ‘Vision in our three-dimensional world''.     

The visual ecology of a deep-sea fish,the escolar Lepidocybium flavobrunneum (Smith, 1843)

Escolar (Lepidocybium flavobrunneum, family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg⁻¹), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.     

Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

Coevolution of visual signals and eye morphology in Polistes paper wasps

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye''s acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.     

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.     

The visual ecology of pupillary action in superposition eyes

The two most common mechanisms of pupillary screening-pigment migration in arthropod superposition eyes are the cone and longitudinal pigment migration mechanisms. The dynamics of each were investigated by optical modelling and by determining experimentally the relationship between eye glow brightness and screening pigment position within the eyes of two representative insect species: the noctuid moth Agrotis infusa and the dung beetle Copris elphenor. During dark adaptation, in both mechanisms, the screening pigment is contracted distally to expose the proximal half of each crystalline cone. During light adaptation the pigment migrates proximally and reduces light flux in the retina. In the longitudinal mechanism, pigment migrates into the clear zone of the eye. In the cone mechanism, pigment never enters the clear zone and is instead restricted to the proximal half of each crystalline cone: a migrating sleeve of pigment creates a small aperture at the end of the crystalline cone, the area of which depends on the degree of light adaptation. According to the model, the cone mechanism provides a limited range of light attenuation (ca. 0.6 log units) for which both good spatial resolution and accuracy of control are maintained, and within this range attenuation is controlled very finely. Beyond this range, whilst attenuation is still possible, diffraction at the pigment aperture and increasing coarseness of control worsen visual performance significantly. In contrast, the longitudinal mechanism provides a much larger useful range of light attenuation (up to several log units) and maintains reasonable fineness of attenuation control over the entire range (although not as fine as the cone mechanism). The experimental results support the model. An extensive survey of arthropods with superposition eyes reveals that the cone mechanism is almost exclusively possessed by those animals experiencing a narrow range of light intensities, and the longitudinal mechanism by those experiencing a wide range.Dedicated to Professor Rolf Elofsson on the occasion of his retirement from the Chair of Zoology in Lund     

The relationship between visual working memory and attention: retention of precise colour information in the absence of effects on perceptual selection

We examined the conditions under which a feature value in visual working memory (VWM) recruits visual attention to matching stimuli. Previous work has suggested that VWM supports two qualitatively different states of representation: an active state that interacts with perceptual selection and a passive (or accessory) state that does not. An alternative hypothesis is that VWM supports a single form of representation, with the precision of feature memory controlling whether or not the representation interacts with perceptual selection. The results of three experiments supported the dual-state hypothesis. We established conditions under which participants retained a relatively precise representation of a parcticular colour. If the colour was immediately task relevant, it reliably recruited attention to matching stimuli. However, if the colour was not immediately task relevant, it failed to interact with perceptual selection. Feature maintenance in VWM is not necessarily equivalent with feature-based attentional selection.     

Led by the nose: Olfaction in primate feeding ecology

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. 1 This view shifted with the growing understanding of its role in social behavior 2 and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory‐dependent mammals such as dogs and rodents. 3 , 4 Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large‐scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates’ feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.     

Game theory and the evolution of fearfulness in wild birds

When animals in a group live under predation threat, the fate of each individual depends on the way it reacts to danger, but also on the behaviour of its companions. Game theory should then help to understand the evolution of fearful behaviour in gregarious animals. To illustrate this approach, a model determines evolutionarily stable levels of fearfulness in bird flocks, assuming that flocks are the object of both predatory attacks and nonlethal disturbance. In the model, high levels of flightiness limit the risk of being killed by predators, but increase the amount of energy lost in flights during the season. The predicted levels of fearfulness are extremely variable. They depend on the respective frequencies of predatory attacks and simple disturbing events, and on the capacity of birds to detect and escape predators. These results may help to explain the variability of flightiness reported in birds.     

The dual function of barred plumage in birds: camouflage and communication

A commonly held principle in visual ecology is that communication compromises camouflage: while visual signals are often conspicuous, camouflage provides concealment. However, some traits may have evolved for communication and camouflage simultaneously, thereby overcoming this functional compromise. Visual patterns generally provide camouflage, but it was suggested that a particular type of visual pattern – avian barred plumage – could also be a signal of individual quality. Here, we test if the evolution of sexual dimorphism in barred plumage, as well as differences between juvenile and adult plumage, indicate camouflage and/or signalling functions across the class Aves. We found a higher frequency of female- rather than male-biased sexual dimorphism in barred plumage, indicating that camouflage is its most common function. But we also found that, compared to other pigmentation patterns, barred plumage is more frequently biased towards males and its expression more frequently restricted to adulthood, suggesting that barred plumage often evolves or is maintained as a sexual communication signal. This illustrates how visual traits can accommodate the apparently incompatible functions of camouflage and communication, which has implications for our understanding of avian visual ecology and sexual ornamentation.     

Distinctive convergence in Australian floral colours seen through the eyes of Australian birds

We used a colour-space model of avian vision to assess whether a distinctive bird pollination syndrome exists for floral colour among Australian angiosperms. We also used a novel phylogenetically based method to assess whether such a syndrome represents a significant degree of convergent evolution. About half of the 80 species in our sample that attract nectarivorous birds had floral colours in a small, isolated region of colour space characterized by an emphasis on long-wavelength reflection. The distinctiveness of this ‘red arm’ region was much greater when colours were modelled for violet-sensitive (VS) avian vision than for the ultraviolet-sensitive visual system. Honeyeaters (Meliphagidae) are the dominant avian nectarivores in Australia and have VS vision. Ancestral state reconstructions suggest that 31 lineages evolved into the red arm region, whereas simulations indicate that an average of five or six lineages and a maximum of 22 are likely to have entered in the absence of selection. Thus, significant evolutionary convergence on a distinctive floral colour syndrome for bird pollination has occurred in Australia, although only a subset of bird-pollinated taxa belongs to this syndrome. The visual system of honeyeaters has been the apparent driver of this convergence.     

Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators

Noise pollution from human traffic networks and industrial activity impacts vast areas of our planet. While anthropogenic noise effects on animal communication are well documented, we have very limited understanding of noise impact on more complex ecosystem processes, such as predator-prey interactions, albeit urgently needed to devise mitigation measures. Here, we show that traffic noise decreases the foraging efficiency of an acoustic predator, the greater mouse-eared bat (Myotis myotis). These bats feed on large, ground-running arthropods that they find by listening to their faint rustling sounds. We measured the bats' foraging performance on a continuous scale of acoustically simulated highway distances in a behavioural experiment, designed to rule out confounding factors such as general noise avoidance. Successful foraging bouts decreased and search time drastically increased with proximity to the highway. At 7.5 m to the road, search time was increased by a factor of five. From this increase, we predict a 25-fold decrease in surveyed ground area and thus in foraging efficiency for a wild bat. As most of the bats' prey are predators themselves, the noise impact on the bats' foraging performance will have complex effects on the food web and ultimately on the ecosystem stability. Similar scenarios apply to other ecologically important and highly protected acoustic predators, e.g. owls. Our study provides the empirical basis for quantitative predictions of anthropogenic noise impacts on ecosystem processes. It highlights that an understanding of the effects of noise emissions and other forms of 'sensory pollution' are crucially important for the assessment of environmental impact of human activities.     

The Drosophila larval visual system: high-resolution analysis of a simple visual neuropil

The task of the visual system is to translate light into neuronal encoded information. This translation of photons into neuronal signals is achieved by photoreceptor neurons (PRs), specialized sensory neurons, located in the eye. Upon perception of light the PRs will send a signal to target neurons, which represent a first station of visual processing. Increasing complexity of visual processing stems from the number of distinct PR subtypes and their various types of target neurons that are contacted. The visual system of the fruit fly larva represents a simple visual system (larval optic neuropil, LON) that consists of 12 PRs falling into two classes: blue-senstive PRs expressing Rhodopsin 5 (Rh5) and green-sensitive PRs expressing Rhodopsin 6 (Rh6). These afferents contact a small number of target neurons, including optic lobe pioneers (OLPs) and lateral clock neurons (LNs). We combine the use of genetic markers to label both PR subtypes and the distinct, identifiable sets of target neurons with a serial EM reconstruction to generate a high-resolution map of the larval optic neuropil. We find that the larval optic neuropil shows a clear bipartite organization consisting of one domain innervated by PRs and one devoid of PR axons. The topology of PR projections, in particular the relationship between Rh5 and Rh6 afferents, is maintained from the nerve entering the brain to the axon terminals. The target neurons can be subdivided according to neurotransmitter or neuropeptide they use as well as the location within the brain. We further track the larval optic neuropil through development from first larval instar to its location in the adult brain as the accessory medulla.     

The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.