Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision

Stomatopod crustaceans have the most complex and diverse assortment of retinal photoreceptors of any animals, with 16 functional classes. The receptor classes are subdivided into sets responsible for ultraviolet vision, spatial vision, colour vision and polarization vision. Many of these receptor classes are spectrally tuned by filtering pigments located in photoreceptors or overlying optical elements. At visible wavelengths, carotenoproteins or similar substances are packed into vesicles used either as serial, intrarhabdomal filters or lateral filters. A single retina may contain a diversity of these filtering pigments paired with specific photoreceptors, and the pigments used vary between and within species both taxonomically and ecologically. Ultraviolet-filtering pigments in the crystalline cones serve to tune ultraviolet vision in these animals as well, and some ultraviolet receptors themselves act as birefringent filters to enable circular polarization vision. Stomatopods have reached an evolutionary extreme in their use of filter mechanisms to tune photoreception to habitat and behaviour, allowing them to extend the spectral range of their vision both deeper into the ultraviolet and further into the red.     

Early duplication and functional diversification of the opsin gene family in insects

Recent analysis of the complete mosquito Anopheles gambiae genome has revealed a far higher number of opsin genes than for either the Drosophila melanogaster genome or any other known insect. In particular, the analysis revealed an extraordinary opsin gene content expansion, whereby half are long wavelength-sensitive (LW) opsin gene duplicates. We analyzed this genomic data in relationship to other known insect opsins to estimate the relative timing of the LW opsin gene duplications and to identify "missing" paralogs in extant species. The inferred branching patterns of the LW opsin gene family phylogeny indicate at least one early gene duplication within insects before the emergence of the orders Orthoptera, Mantodea, Hymenoptera, Lepidoptera, and Diptera. These data predict the existence of one more LW opsin gene than is currently known from most insects. We tested this prediction by using a degenerate PCR strategy to screen the hymenopteran genome for novel LW opsin genes. We isolated two LW opsin gene sequences from each of five bee species, Bombus impatiens, B. terrestris, Diadasia afflicta, D. rinconis, and Osmia rufa, including 1.1 to 1.2 kb from a known (LW Rh1) and 1 kb from a new opsin gene (LW Rh2). Phylogenetic analysis suggests that the novel hymenopteran gene is orthologous to A. gambiae GPRop7, a gene that is apparently missing from D. melanogaster. Relative rate tests show that LW Rh2 is evolving at a slower rate than LW Rh1 and, therefore, may be a useful marker for higher-level hymenopteran systematics. Site-specific rate tests indicate the presence of several amino acid sites between LW Rh1 and LW Rh2 that have undergone shifts in selective constraints after duplication. These sites and others are discussed in relationship to putative structural and functional differences between the two genes.     

Eye shape and the nocturnal bottleneck of mammals

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. By contrast, several studies have concluded that many mammals exhibit typical nocturnal eye shapes, regardless of activity pattern. However, a recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night). Here, we conduct a detailed analysis of eye shape and activity pattern in mammals, using a broad comparative sample of 266 species. We find that the eye shapes of cathemeral mammals completely overlap with nocturnal and diurnal species. Additionally, most diurnal and cathemeral mammals have eye shapes that are most similar to those of nocturnal birds and lizards. The only mammalian clade that diverges from this pattern is anthropoids, which have convergently evolved eye shapes similar to those of diurnal birds and lizards. Our results provide additional evidence for a nocturnal ‘bottleneck’ in the early evolution of crown mammals.     

Cuttlefish see shape from shading,fine-tuning coloration in response to pictorial depth cues and directional illumination

Humans use shading as a cue to three-dimensional form by combining low-level information about light intensity with high-level knowledge about objects and the environment. Here, we examine how cuttlefish Sepia officinalis respond to light and shadow to shade the white square (WS) feature in their body pattern. Cuttlefish display the WS in the presence of pebble-like objects, and they can shade it to render the appearance of surface curvature to a human observer, which might benefit camouflage. Here we test how they colour the WS on visual backgrounds containing two-dimensional circular stimuli, some of which were shaded to suggest surface curvature, whereas others were uniformly coloured or divided into dark and light semicircles. WS shading, measured by lateral asymmetry, was greatest when the animal rested on a background of shaded circles and three-dimensional hemispheres, and less on plain white circles or black/white semicircles. In addition, shading was enhanced when light fell from the lighter side of the shaded stimulus, as expected for real convex surfaces. Thus, the cuttlefish acts as if it perceives surface curvature from shading, and takes account of the direction of illumination. However, the direction of WS shading is insensitive to the directions of background shading and illumination; instead the cuttlefish tend to turn to face the light source.     

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.     

Comparative analysis of the size and shape of the lizard eye

Lizards occupy both scotopic (light-limited) and photopic (light-rich) environments, thereby making this clade ideal for analyses of eye morphology adaptations. This study examines how in lizards the morphology of the eye varies according to activity in these different light environments. Measurements were collected on corneal diameters and axial lengths of the eye for 239 specimens of 116 lizard species (including Sphenodon) that include both species with scotopic and photopic visual adaptations. I show that the light level available to a lizard for vision has a significant effect on eye shape and size. Scotopic lizards have eye shapes that are optimized for visual sensitivity, with larger corneal diameters relative to axial lengths. However, photopic lizards do not exhibit absolutely larger axial lengths than do scotopic lizards, and the groups have the same absolute axial lengths of the eye. Results also indicate that the light level the lizard functions under is a more significant influence on eye shape, as defined by the relationship between corneal diameter and axial length of the eye, than is phylogeny.     

Guanine and its retinal distribution in the tapetum of the bigeye tuna,thunnus obesus

The eye of the bigeye tuna (Thunnus obesus) contains a retinal tapetum composed of guanine. The total amount of the guanine in one eye of the fish (SL=120 cm) was about 88.6 mg. The mean guanine content of the tapetum was approximately 1.25 mg/cm² of the retinal surface. The highest content of guanine (2.15 mg/cm²) was observed only in the ventro-temporal part of the retina. To distinguish this area from the rest of the eye, we suggested the term ‘locus tapetalis’ for it. The visual accommodation system clearly indicated that the visual axis of the fish is upper-forward and the resulting retinal area for acute vision was suggested to be in the ventro-temporal retina. We discussed that the area centralis of the bigeye tuna may have two functions: to guarantee high visual acuity and to allow for high photo-sensitivity in dim light vision.     

Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies

Butterfly long-wavelength (L) photopigments are interesting for comparative studies of adaptive evolution because of the tremendous phenotypic variation that exists in their wavelength of peak absorbance (lambda(max) value). Here we present a comprehensive survey of L photopigment variation by measuring lambda(max) in 12 nymphalid and 1 riodinid species using epi-microspectrophotometry. Together with previous data, we find that L photopigment lambda(max) varies from 510-565 nm in 22 nymphalids, with an even broader 505- to 600-nm range in riodinids. We then surveyed the L opsin genes for which lambda(max) values are available as well as from related taxa and found 2 instances of L opsin gene duplication within nymphalids, in Hermeuptychia hermes and Amathusia phidippus, and 1 instance within riodinids, in the metalmark butterfly Apodemia mormo. Using maximum parsimony and maximum likelihood ancestral state reconstructions to map the evolution of spectral shifts within the L photopigments of nymphalids, we estimate the ancestral pigment had a lambda(max) = 540 nm +/- 10 nm standard error and that blueshifts in wavelength have occurred at least 4 times within the family. We used ancestral state reconstructions to investigate the importance of several amino acid substitutions (Ile17Met, Ala64Ser, Asn70Ser, and Ser137Ala) previously shown to have evolved under positive selection that are correlated with blue spectral shifts. These reconstructions suggest that the Ala64Ser substitution has indeed occurred along the newly identified blueshifted L photopigment lineages. Substitutions at the other 3 sites may also be involved in the functional diversification of L photopigments. Our data strongly suggest that there are limits to the evolution of L photopigment spectral shifts among species with only one L opsin gene and that opsin gene duplication broadens the potential range of lambda(max) values.