Molecular ecology and adaptation of visual photopigments in craniates

Abstract

In craniates, opsin-based photopigments expressed in the eye encode molecular 'light sensors' that constitute the initial protein in photoreception and the activation of the phototransduction cascade. Since the cloning and sequencing of the first vertebrate opsin gene (bovine rod opsin) nearly 30 years ago (Ovchinnikov Yu 1982, FEBS Letters, 148, 179-191; Hargrave et al. 1983, Biophysics of Structure & Mechanism, 9, 235-244; Nathans & Hogness 1983, Cell, 34, 807-814), it is now well established that variation in the subtypes and spectral properties of the visual pigments that mediate colour and dimlight vision is a prevalent mechanism for the molecular adaptation to diverse light environments. In this review, we discuss the origins and spectral tuning of photopigments that first arose in the agnathans to sample light within the ancient aquatic landscape of the Early Cambrian, detailing the molecular changes that subsequently occurred in each of the opsin classes independently within the main branches of extant jawed gnathostomes. Specifically, we discuss the adaptive changes that have occurred in the photoreceptors of craniates as they met the ecological challenges to survive in quite differing photic niches, including brightly lit aquatic surroundings; the deep sea; the transition to and from land; diurnal, crepuscular and nocturnal environments; and lightrestricted fossorial settings. The review ends with a discussion of the limitations inherent to the 'nocturnal-bottleneck' hypothesis relevant to the evolution of the mammalian visual system and a proposition that transition through a 'mesopic-bottleneck' may be a more appropriate model.

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

“…MSP and in vitro regeneration), this study has demonstrated that five opsin genes encoding a rod and four cone visual pigments are expressed in the retina of P. elegans adelaidae. These opsin genes are orthologous to the pigments classes found in other birds and the vertebrates in general (Yokoyama, 2000a;Davies et al, 2012). Although visual pigments present in many avian species have been identified, only in three species [the chicken (Okano et al, 1992), the pigeon (Kawamura et al, 1999) and the zebra finch (Taeniopygia guttata) (Yokoyama et al, 2000)] have the full complement of rod and cone opsin genes been identified and sequenced.…”

“…Specifically, the presence of S164/H181/Y261/T269/A292 (SHYTA) typically yields a pigment with a λ max value at 560 nm (Yokoyama, 2000a;Davies et al, 2012). Despite the presence of SHYTA in P. elegans, the λ max value determined by MSP was long-wavelength shifted at 567 nm (Fig.…”

“…MWS cones may contain either an SWS2, an RH2 or an LWS pigment (Davies et al, 2012)]. Therefore, it is important to establish the genetic basis for the different cone classes present in the P. elegans retina.…”

“…Opsins are G protein-coupled receptors (GPCRs) that are rendered light sensitive by the Schiff base linkage of the chromophore, retinal, to a lysine residue at site 296 (Yokoyama, 2000a;Davies et al, 2012). In the opsin, amino acids present at specific sites are known to 'tune' the peak spectral sensitivity of the visual pigment to particular wavelengths (Yokoyama, 2000a;Davies et al, 2012); variation at these tuning sites may underlie, therefore, any intraspecific variation in absorbance spectra in P. elegans. The SWS1 opsin gene sequence of P. elegans has been reported previously and has been shown to encode a UV-sensitive pigment (Carvalho et al, 2011).…”

Genomic evidence for rod monochromacy in sloths and armadillos suggests early subterranean history for Xenarthra

“…Electrophysiological, molecular and genetic techniques have greatly increased our knowledge of the retinal basis for vision in mammals [1][2][3][4]. Cone photoreceptorsresponsible for high acuity, colour vision in bright light-typically possess one of four spectral classes of photopigment called opsins.…”