Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution

Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.

The visual ecology of avian photoreceptors

The spectral sensitivities of avian retinal photoreceptors are examined with respect to microspectrophotometric measurements of single cells, spectrophotometric measurements of extracted or in vitro regenerated visual pigments, and molecular genetic analyses of visual pigment opsin protein sequences. Bird species from diverse orders are compared in relation to their evolution, their habitats and the multiplicity of visual tasks they must perform. Birds have five different types of visual pigment and seven different types of photo receptor-rods, double (uneven twin) cones and four types of single cone. The spectral locations of the wavelengths of maximum absorbance (lambda (max)) of the different visual pigments, and the spectral transmittance characteristics of the intraocular spectral filters (cone oil droplets) that also determine photoreceptor spectral sensitivity, vary according to both habitat and phylogenetic relatedness. The primary influence on avian retinal design appears to be the range of wavelengths available for vision, regardless of whether that range is determined by the spectral distribution of the natural illumination or the spectral transmittance of the ocular media (cornea, aqueous humour, lens, vitreous humour). Nevertheless, other variations in spectral sensitivity exist that reflect the variability and complexity of avian visual ecology. (C) 2001 Elsevier Science Ltd. All rights reserved.

Vision in the peafowl (Aves : Pavo cristatus)

The visual sense of the Indian blue-shouldered peafowl Pavo cristatus was investigated with respect to the spectral absorption characteristics of the retinal photoreceptors, the spectral transmittance of the ocular media and the topographic distribution of cells in the retinal ganglion cell layer. Microspectrophotometry revealed a single class of rod, four spectrally distinct types of single cone and a single class of double cone. In the case of the single cone types, which contained visual pigments with wavelengths of maximum absorbance (lambda(max)) at 424, 458, 505 and 567 nm, spectral filtering by the ocular media and the different cone oil droplets with which each visual pigment is associated gives predicted peak spectral sensitivities of 432, 477, 537 and 605 nm, respectively. Topographic analysis of retinal ganglion cell distribution revealed a large central area of increased cell density (at peak, 35,609 cells mm(-2)) with a poorly defined visual streak extending nasally. The peafowl has a calculated maximum spatial resolution (visual acuity) in the lateral visual field of 20.6 cycles degrees(-1). These properties of the peafowl eye are discussed with respect to its visual ecology and are compared with those of other closely related species.

Long-term potentiation of synaptic transmission in the avian hippocampus

The avian hippocampus plays a pivotal role in memory required for spatial navigation and food storing. Here we have examined synaptic transmission and plasticity within the hippocampal formation of the domestic chicken using an in vitro slice preparation. With the use of sharp microelectrodes we have shown that excitatory synaptic inputs in this structure are glutamatergic and activate both NMDA-and AMPA-type receptors on the postsynaptic membrane. In response to tetanic stimulation, the EPSP displayed a robust long-term potentiation (LTP) lasting >1 hr. This LTP was unaffected by blockade of NMDA receptors or chelation of postsynaptic calcium. Application of forskolin increased the EPSP and reduced paired-pulse facilitation: (PPF), indicating an increase in release probability. In contrast, LTP was not associated with a change in the PPF ratio. Induction of LTP did not occlude the effects of forskolin. Thus, in contrast to NMDA receptor-independent LTP in the mammalian brain, LTP in the chicken hippocampus is not attributable to a change in the probability of transmitter release and does not require activation of adenylyl cyclase, These findings indicate that a novel form of synaptic plasticity might underlie learning in the avian hippocampus.

Tetrachromacy, oil droplets and bird plumage colours

There is a growing body of data on avian eyes, including measurements of visual pigment and oil droplet spectral absorption, and of receptor densities and their distributions across the retina. These data are sufficient to predict psychophysical colour discrimination thresholds for light-adapted eyes, and hence provide a basis for relating eye design to visual needs. We examine the advantages of coloured oil droplets, UV vision and tetrachromacy for discriminating a diverse set of avian plumage spectra under natural illumination. Discriminability is enhanced both by tetrachromacy and coloured oil droplets. Oil droplets may also improve colour constancy. Comparison of the performance of a pigeon's eye, where the shortest wavelength receptor peak is at 410 nm, with that of the passerine Leiothrix, where the ultraviolet-sensitive peak is at 365 nm, generally shows a small advantage to the latter, but this advantage depends critically on the noise level in the sensitivity mechanism and on the set of spectra being viewed.

Inhibition of transmitter release and long-term depression in the avian hippocampus

Long-term depression has recently been shown to occur at glutamatergic synapses in the avian hippocampus and requires activation of calcium/calmodulin-dependent protein kinase II in the nerve terminal. Here using whole cell and intracellular recordings from brain slices, we show that the N-type calcium channel contributes significantly to glutamate release in the avian hippocampus. Activation of the metabotrobic gamma-aminobutyric acid (GABA)(B) receptor by the specific agonist baclofen blocks synaptic transmission. The action of baclofen was associated with a change in paired pulse facilitation indicating that it resulted from a reduction in the probability of transmitter release, In contrast, no change in paired pulse facilitation was observed following the induction of long-term depression. These results show that activation of GABA(B) receptors and long-term depression reduce transmitter release by distinct mechanisms. (C) 2000 Elsevier Science Ireland Ltd. All rights reserved.

Colour vision in billfish

Members of the billfish family are highly visual predatory teleosts inhabiting the open ocean. Little is known about their visual abilities in detail, but past studies have indicated that these fishes were:ere likely to be monochromats. This study however, presents evidence of two anatomically distinct cone types in billfish. The cells are arranged in a regular mosaic pattern of single and twin cones as in many fishes, and this arrangement suggests that the different cone types also show different spectral sensitivity, which is the basis for colour vision. First measurements using microspectrophotometry (MSP) revealed a peak absorption of the rod pigment at 484 nm, indicating that MSP, despite technical difficulties, will be a decisive tool in proving colour vision in these offshore fishes. When hunting, billfish such as the sailfish flash bright blue bars on their sides. This colour reflects largely in ultraviolet (UV) light at 350 nm as revealed by spectrophotometric measurements. Billfish lenses block light of wavelengths below 400 nm, presumably rendering the animal blind to the UV component of its own body colour. Interestingly at least two prey species of billfish have lenses transmitting light in the UV waveband and are therefore likely to perceive a large fraction of the UV peak found in the blue bar of the sailfish. The possible biological significance of this finding is discussed.

Neuroarchitecture of the color and polarization vision system of the stomatopod haptosquilla

The apposition compound eyes of stomatopod crustaceans contain a morphologically distinct eye region specialized for color and polarization vision, called the mid-band. In two stomatopod superfamilies, the mid-band is constructed from six rows of enlarged ommatidia containing multiple photoreceptor classes for spectral and polarization vision. The aim of this study was to begin to analyze the underlying neuroarchitecture, the design of which might reveal clues how the visual system interprets and communicates to deeper levels of the brain the multiple channels of information supplied by the retina. Reduced silver methods were used to investigate the axon pathways from different retinal regions to the lamina ganglionaris and from there to the medulla externa, the medulla interna, and the medulla terminalis. A swollen band of neuropil-here termed the accessory lobe-projects across the equator of. the lamina ganglionaris, the medulla externa, and the medulla interna and represents, structurally, the retina's mid-band. Serial semithin and ultrathin resin sections were used to reconstruct the projection of photoreceptor axons from the retina to the lamina ganglionaris. The eight axons originating from one ommatidium project to the same lamina cartridge. Seven short visual fibers end at two distinct levels in each lamina cartridge, thus geometrically separating the two channels of polarization and spectral information. The eighth visual fiber runs axially through the cartridge and terminates in the medulla externa. We conclude that spatial, color, and polarization information is divided into three parallel data streams from the retina to the central nervous system. (C) 2003 Wiley-Liss, Inc.

Polarization vision and its role in biological signaling

Visual pigments, the molecules in photoreceptors that initiate the process of vision, are inherently dichroic, differentially absorbing light according to its axis of polarization. Many animals have taken advantage of this property to build receptor systems capable of analyzing the polarization of incoming light, as polarized light is abundant in natural scenes (commonly being produced by scattering or reflection). Such polarization sensitivity has long been associated with behavioral tasks like orientation or navigation. However, only recently have we become aware that it can be incorporated into a high-level visual perception akin to color vision, permitting segmentation of a viewed scene into regions that differ in their polarization. By analogy to color vision, we call this capacity polarization vision. It is apparently used for tasks like those that color vision specializes in: contrast enhancement, camouflage breaking, object recognition, and signal detection and discrimination. While color is very useful in terrestrial or shallow-water environments, it is an unreliable cue deeper in water due to the spectral modification of light as it travels through water of various depths or of varying optical quality. Here, polarization vision has special utility and consequently has evolved in numerous marine species, as well as at least one terrestrial animal. In this review, we consider recent findings concerning polarization vision and its significance in biological signaling.