The sequences of the SWS1
opsin gene presented here for a total of 14 Neotropical, Australasian and African species sampled across the Psittacidae, Cacatuidae and Nestoridae families, show that all have Cys90. Previous studies by Wilkie et al
] and Yokoyama et al
] have shown that in avian pigments, the presence of Cys90 confers UV sensitivity, whereas VS pigments from other species have Ser90. Furthermore, the in vitro
-expressed rosella SWS1
pigment gave a peak at 363 nm, thereby confirming the presence of UVS pigments in the larger and longer lived parrot species. The Psittaciformes are therefore the only avian order where all species studied to date have a UVS pigment and is strong evidence that the Ser90Cys substitution responsible for this peak shift into the UV occurred at the base of the Psittaciformes lineage, and has been retained in all extant species.
Consistent with the presence of UVS pigments, the lens of P. elegans
has a 50 per cent transparency cut-off at around 320 nm, which would allow a substantial proportion of UV light to reach the retina. This rises to 76 per cent transmission at the peak sensitivity of 363 nm of the expressed pigment. Coloured oil droplets that act as cut-off filters are routinely found in avian single cones. The cut-off wavelengths of these droplets are matched to the spectral sensitivity of the different cone pigments [12
] and would therefore offer some protection to photoreceptor outer segments. UVS cones however have T-type (transparent) droplets that show no detectable absorbance from 330 to 800 nm, so these droplets would not significantly reduce the penetration of UV light into the outer segments of UVS photoreceptors. Nevertheless, all photoreceptor cells would be exposed to transmitted UV light proximal to the oil droplets; thus, the need for photoprotection for the nucleus and other organelles proximal to the oil droplets might be similar for all photoreceptor types, and indeed for many cell types in the retina. Whether long-lived birds compared with short-lived birds have increased lipopigment in the retinal pigment epithelium, or better mechanisms for removal of peroxidized lipids in the outer segments, remains to be determined.
The selective pressures that were responsible for the re-acquisition of UVS pigments in birds are unclear. The SWS1
opsin sequences for the 14 parrot species reported here are highly conserved: when compared with the budgerigar sequence, only a small number of nucleotide differences are observed, with very few of these differences being non-synonymous. A better understanding of the visual ecology of these birds will be essential in determining how UV sensitivity is employed. UV-reflecting plumages are found ubiquitously across all avian lineages, including parrots, suggesting that UV reflectance is an ancestral characteristic of the avian order [27
]. The highest percentage (more than 10%) of UV reflectance is usually found in blue and white feathers, although feathers reflecting predominantly at longer wavelengths can have a biologically significant UV reflectance [28
]. Parrots have the highest percentage of UV reflectance, especially in plumage patches when compared with all other avian orders, and in a survey of 143 species, all but three were shown to possess a considerable amount of UV-reflecting plumage [48
With the exception of P. elegans
that has an expected lifespan of around 15–20 years in captivity, all the other species investigated here are considered long-lived with lifespan of up to 50 years or more in captivity [37
]. UV radiation is known to damage several components of the eye such as the cornea, lens, the retinal pigment epithelium and the photoreceptors, leading to apoptosis in the cornea and pigment epithelium [33
], decreased lens cell viability [50
], the induction of oxidative stress [52
] and the inactivation of anti-oxidant enzymes like catalase [34
]. UV radiation is also associated with several age-related conditions like cataract and macular degeneration [33
]. In mammals, a long lifespan would appear to be associated with a loss of UV-sensitivity of the visual system with the peak sensitivities of the SWS1 pigments shifted to wavelengths greater than 400 nm [11
]. Only short-lived species such as the rat and mouse among the Eutheria have retained UVS pigments although, from the species studied so far, this may be more prevalent among the metatheria [3
]. The penetration of UV radiation in the neural retina in long-lived parrot species might be expected therefore to cause irreversible damage [34
] and raises the question as to how these species tolerate UV exposure. One explanation may be that birds show a lower rate of mitochondrial free-radical production in comparison with mammals [53
]. Furthermore, cells of long-lived birds exhibit exceptional resistance to oxidative-induced damage when compared with shorter-lived birds and mammals [55
], although the underlying genetic and molecular basis for this higher oxidative resistance is unknown. A third explanation could be the presence of carotenoids, which are present not only in the oil droplets of the retina, but also in the serum of parrots at concentrations comparable to that in other bird species [12
]. Carotenoids are known to be effective antioxidants and immunostimulants in birds (reviewed in [57
]), with lutein and zeaxanthin being especially effective in conferring protection against oxidative damage in the retina [58
] and light-induced photoreceptor apoptosis [60
]. Similarly, psittacofulvin pigments, found so far only in parrot feathers, are thought to have considerable antioxidant properties [61
], and could offer protection if also present in the retina.
If such processes are occurring in the retina, the combination of a lower production of free radicals and an increased resistance to oxidative damage could protect the eye against the damaging effects of UV light exposure in long-lived parrot species. A more detailed study of these potential protection mechanisms could provide valuable information on the survival of retinal cells. Such studies would reveal not only how extant long-lived diurnal terrestrial birds avoid UV-induced photodamage, but may also give new insights into UV protection, thereby facilitating improvements in human health associated with reducing or ameliorating UV-induced photodamage.