Functional characterization of spectral tuning mechanisms in the great bowerbird short-wavelength sensitive visual pigment (SWS1), and the origins of UV/violet vision in passerines and parrots

Abstract

BackgroundOne of the most striking features of avian vision is the variation in spectral sensitivity of the short wavelength sensitive (SWS1) opsins, which can be divided into two sub-types: violet- and UV- sensitive (VS & UVS). In birds, UVS has been found in both passerines and parrots, groups that were recently shown to be sister orders. While all parrots are thought to be UVS, recent evidence suggests some passerine lineages may also be VS. The great bowerbird (Chlamydera nuchalis) is a passerine notable for its courtship behaviours in which males build and decorate elaborate bower structures.ResultsThe great bowerbird SWS1 sequence possesses an unusual residue combination at known spectral tuning sites that has not been previously investigated in mutagenesis experiments. In this study, the SWS1 opsin of C. nuchalis was expressed along with a series of spectral tuning mutants and ancestral passerine SWS1 pigments, allowing us to investigate spectral tuning mechanisms and explore the evolution of UV/violet sensitivity in early passerines and parrots. The expressed C. nuchalis SWS1 opsin was found to be a VS pigment, with a λmax of 403 nm. Bowerbird SWS1 mutants C86F, S90C, and C86S/S90C all shifted λmax into the UV, whereas C86S had no effect. Experimentally recreated ancestral passerine and parrot/passerine SWS1 pigments were both found to be VS, indicating that UV sensitivity evolved independently in passerines and parrots from a VS ancestor.ConclusionsOur mutagenesis studies indicate that spectral tuning in C. nuchalis is mediated by mechanisms similar to those of other birds. Interestingly, our ancestral sequence reconstructions of SWS1 in landbird evolution suggest multiple transitions from VS to UVS, but no instances of the reverse. Our results not only provide a more precise prediction of where these spectral sensitivity shifts occurred, but also confirm the hypothesis that birds are an unusual exception among vertebrates where some descendants re-evolved UVS from a violet type ancestor. The re-evolution of UVS from a VS type pigment has not previously been predicted elsewhere in the vertebrate phylogeny.

Cone-like rhodopsin expressed in the all cone retina of the colubrid pine snake as a potential adaptation to diurnality

“…2B), which is similar to the measured λ max of rhodopsins from T. proximus, T. sirtalis and Arizona elegans snakes (Schott et al, 2016;Sillman et al, 1997;Simões et al, 2016). The drastic blue shift is expected given the presence of the blue-shifting N83 and S292 amino acid identities (Bickelmann et al, 2012;Dungan et al, 2016;van Hazel et al, 2016). Pituophis melanoleucus rhodopsin expression was similar to that of T. proximus, with a large ratio between total purified protein (absorbance at 280 nm) and active protein (absorbance at λ max ) that indicates that only a small proportion of the translated opsin protein is able to bind chromophore and become functionally active.…”

“…Mutations at site 185 have been shown to reduce both visual pigment stability (McKibbin et al, 2007) and transducin activation in vitro (Karnik et al, 1988). Also, the P. melanoleucus RH1 has N83 and S292, which are often found in rhodopsins with blue-shifted λ max values, and can also affect all-trans retinal release kinetics following photoactivation (Bickelmann et al, 2012;van Hazel et al, 2016).…”

“…Expression vectors containing P. melanoleucus cone opsin and rhodopsin genes were transiently transfected into cultured HEK293T cells (ATCC CRL-11268) using Lipofectamine 2000 (Invitrogen; 8 µg of DNA per 10-cm plate) and harvested after 48 h. Visual pigments were regenerated with 11-cis retinal, generously provided by Dr Rosalie Crouch (Medical University of South Carolina), solubilized in 1% dodecylmaltoside, and purified with the 1D4 monoclonal antibody (University of British Columbia 95-062, lot 1017; Molday and MacKenzie, 1983) as previously described Chang, 2015, 2010;Morrow et al, 2011). RH1 and SWS1 pigments were purified in sodium phosphate buffers and LWS was purified in HEPES buffers containing glycerol (as described in van Hazel et al, 2013). The ultravioletvisible absorption spectra of purified visual pigments were recorded using a Cary 4000 double beam spectrophotometer (Agilent, Santa Clara, CA, USA).…”

The evolution of opsins and color vision: connecting genotype to a complex phenotype

“…The effects of many substitutions on the spectral tuning of the different visual pigment types has been investigated. This has been accomplished by comparing the visual pigments of different species (Yokoyama and Yokoyama, 1996;Yokoyama et al, 2008a;Bloch et al, 2015a;Bloch et al, 2015b) and conducting sophisticated site-directed mutagenesis experiments (Yokoyama, 2000;van Hazel et al, 2013). The combination of phylogenetic methods to identify key substitution that occur multiple times throughout vertebrate evolution, site-directed mutagenesis to introduce and reverse those substitutions in visual pigments and in vitro expression has contributed immensely to our understanding of spectral tuning.…”

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

“…Although considerable progress has been made in the study of the distribution and variability of UV photoreceptors in birds (e.g. Hart and Hunt, 2007;Ödeen et al, 2011;Ödeen et al, 2012;Carvalho et al, 2012;Coyle et al, 2012;Ödeen and Håstad, 2013;van Hazel et al, 2013) and fish (e.g. Carleton et al, 2000;Siebeck and Marshall, 2001;Siebeck and Marshall, 2007;Siebeck et al, 2010), data on other vertebrate linages are relatively scant and encompass few species [e.g.…”