Visual Pigment Evolution in Reptiles

Abstract

The long history and great ecological and morphological diversity of reptiles (all amniotes except mammals and birds) is matched by their visual system diversity. Although less known than in other amniotes, visual pigments have been studied in all extant reptile orders except Sphenodontia. There have been no additions to the five visual pigments present in the ancestral vertebrate, although there have been multiple independent losses. Crocodylians retain three visual pigments, many lizards as well as Testudines four or five and snakes one to three. Adaptive pigment evolution includes tuning site amino acid substitutions and switches between chromophore types that together generate ultraviolet to infrared spectral sensitivity. Reptiles present some of the best evidences of evolutionary rod–cone and cone–rod transmutation with, for example typically cone visual pigments expressed in rod‐like photoreceptors. Reptile visual pigments show evidence of substantial adaptive evolution, at least some of which is associated with major ecological shifts. Key Concepts Reptiles have no more than five visual pigments, as few as one and typically at least three. Up to four of the ancestral vertebrate visual pigments have been lost independently in different reptile lineages, and no visual opsin gene duplications have been identified so far. Testudines have between four and five visual pigments and a wide range of photoreceptor oil droplets, representing one of the most complex visual pigment systems in tetrapod vertebrates. Despite many of them being nocturnal, no rhodopsin 1 has been detected in geckos. No sws1 or rh2 opsin genes can be detected in genomic sequence data for crocodylians. Among squamates, some lizards have a mixture of A 1 and A 2 chromophores incorporated in their visual pigments, allowing a wide colour sensitivity, including infrared vision. In the green anole ( Anolis carolinensis ), only cone opsins have been reported (SWS1, SWS2, RH2 and LWS) in studies of the eye. However, a 515‐nm tuned rh1 rhodopsin gene occurs in the genome of this species. Extant snakes have lost two visual pigments (SWS2 and RH2), likely as an adaptation to a low light environment inhabited by a snake ancestor. Extreme burrowing in scolecophidians (blind, worm and thread snakes) is correlated with the loss of the SWS1 and LWS visual pigments and cones, rendering these snakes rod (RH1) monochromats. The expression of RH1, SWS1 and LWS pigments in snake lineages with seemingly all‐cone and all‐rod retinae suggests multiple transmutations from cone to rod and vice versa in snakes. Similar transmutations likely occurred in some lizards and perhaps crocodylians. Visual pigment spectral sensitivity in reptiles has been found to correlate with the light transmission properties of the ocular media (e.g. snakes) and photoreceptor oil droplets (e.g. testudines), that is the pigments are not sensitive to wavelengths of light filtered out by these structures.

Opsin-based photopigments expressed in the retina of a South American pit viper,Bothrops atrox(Viperidae)

“…By contrast, the other two opsin classes, namely SWS2 and RH2, which are expressed in many other reptiles, but have never been identified in snakes, were not identified. This is consistent with the likely loss of these genes in the ancestor to all snakes, including their omission from two sequenced snake genomes (Castoe et al, 2013;Simões et al, 2015;Simões & Gower, 2017;Vonk et al, 2013). This is an identical complement of opsin genes to both "lower order" (i.e., more ancestral) and "higher order" snakes, except for the burrowing blind snakes of the Order Scolecophidia, where only RH1 is present (Davies et al, 2009b;Simões et al, 2015).…”

The pupillary light responses of animals; a review of their distribution, dynamics, mechanisms and functions

“…Reptilia is sometimes used as a name for a monophyletic group comprising 'reptiles' and birds (e.g. Simões & Gower, 2017).…”

The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

“…Although this is a topic that has been reviewed relatively recently (Simões and Gower, 2017), many scientific articles have been published within the past 2 years, especially regarding the visual system of snakes and other non-squamate reptiles. Therefore, this more up-to-date review is provided to synthesize these latest studies within a wider context of reptilian visual photobiology.…”

“…recently by Simões and Gower (2017), many studies have been published since that publication, primarily investigating the visual system of snakes (Bhattacharyya et al, 2017;Hauzman et al, 2017;Katti et al, 2018;Schott et al, 2018;Bittencourt et al, 2019;Gower et al, 2019;among others); thus shedding more light on the visual system and the activity patterns of these animals. In addition, this review forms part of a special Research (Themed) Topic ("Multiplicity of physiological systems that detect light or are regulated by photic information").…”