Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity

Abstract

SUMMARY The cone photoreceptors of many vertebrates contain spherical organelles called oil droplets. In birds, turtles, lizards and some lungfish the oil droplets are heavily pigmented and function to filter the spectrum of light incident upon the visual pigment within the outer segment. Pigmented oil droplets are beneficial for colour discrimination in bright light, but at lower light levels the reduction in sensitivity caused by the pigmentation increasingly outweighs the benefits generated by spectral tuning. Consequently, it is expected that species with pigmented oil droplets should modulate the density of pigment in response to ambient light intensity and thereby regulate the amount of light transmitted to the outer segment. In this study, microspectrophotometry was used to measure the absorption spectra of cone oil droplets in chickens (Gallus gallus domesticus) reared under bright (unfiltered) or dim (filtered) sunlight. Oil droplet pigmentation was found to be dependent on the intensity of the ambient light and the duration of exposure to the different lighting treatments. In adult chickens reared in bright light, the oil droplets of all cone types (except the violet-sensitive single cones, whose oil droplet is always non-pigmented) were more densely pigmented than those in chickens reared in dim light. Calculations show that the reduced levels of oil droplet pigmentation in chickens reared in dim light would increase the sensitivity and spectral bandwidth of the outer segment significantly. The density of pigmentation in the oil droplets presumably represents a trade-off between the need for good colour discrimination and absolute sensitivity. This might also explain why nocturnal animals, or those that underwent a nocturnal phase during their evolution, have evolved oil droplets with low pigment densities or no pigmentation or have lost their oil droplets altogether.

How parrots see their colours: novelty in the visual pigments ofPlatycercus elegans

“…If so, rigorous physiological and behavioural measurements will be necessary to determine whether ocular responses and visual behaviours differ between avian species (and subspecies) that possess these features when compared with those species (or subspecies) that express the traditional opsins found in the birds studied to date. Additionally, the oil droplets located in bird retinas have a marked beneficial effect on colour resolution and colour constancy in birds (Vorobyev et al, 1998;Vorobyev, 2003;Knott et al, 2010;Knott et al, 2012), and are known to vary in response to diet (Bowmaker et al, 1993;Knott et al, 2010) and light environment (Hart et al, 2006). These oil droplets could potentially show consistent absorbance differences between P. elegans subspecies that could thereby cause intraspecific variation in vision.…”

Limited variation in visual sensitivity among bowerbird species suggests that there is no link between spectral tuning and variation in display colouration

“…Hart, 2004;Hart et al, 2006). Experimental evidence suggests that the more dense pigmentation of oil droplets in cones of the ventral retina may function to buffer the greater intensity of downwelling light that they receive compared with cones in the dorsal retina (Hart et al, 2006).…”

Morphology, Characterization and Distribution of Retinal Photoreceptors in the South American (Lepidosiren paradoxa) and Spotted African (Protopterus dolloi) Lungfishes

“…Many species of vertebrates contain colorless oil droplets, such as the turtle Pseudymys scripta (Kolb and Jones, 1987), the green frog Rana clamitans (Hailman, 1976), and the strawberry poison frog Dendrobates pumilio (Siddiqi et al, 2004). It is speculated that retinal oil droplets were originally colored, but where species have subsequently become nocturnal these pigments were lost (Hart et al, 2006). This is presumably because the benefits of spectral tuning conferred by colored oil droplets are outweighed by the reduction in absolute sensitivity that would make vision in dim light more difficult.…”

“…This is presumably because the benefits of spectral tuning conferred by colored oil droplets are outweighed by the reduction in absolute sensitivity that would make vision in dim light more difficult. Chickens (Gallus gallus domesticus) reared in dim light develop less dense pigmentation in their colored oil droplets compared to those reared in bright light, presumably to maintain absolute sensitivity at the expense of spectral tuning (Hart et al, 2006), so it may be possible that adopting nocturnality provided the selective pressure to lose colored pigments within oil droplets. All oil droplets can potentially act as micro-lenses to increase photon capture (Sivak et al, 1999); although more research is needed to determine what role they play in P. dolloi and L. paradoxa.…”