Daily activity patterns influence retinal morphology, signatures of selection, and spectral tuning of opsin genes in colubrid snakes

Abstract

BackgroundMorphological divergences of snake retinal structure point to complex evolutionary processes and adaptations. The Colubridae family has a remarkable variety of retinal structure that can range from all-cone and all-rod to duplex (cone/rod) retinas. To explore whether nocturnal versus diurnal activity is responsible for constraints on molecular evolution and plays a role in visual opsin spectral tuning of colubrids, we carried out molecular evolution analyses of the visual opsin genes LWS, RH1, and SWS1 from 17 species and performed morphological analyses.ResultsPhylogenetic reconstructions of the RH1 and LWS recovered major clades characterized by primarily diurnal or primarily nocturnal activity patterns, in contrast with the topology for SWS1, which is very similar to the species tree. We found stronger signals of purifying selection along diurnal and nocturnal lineages for RH1 and SWS1, respectively. A blue-shift of the RH1 spectral peak is associated with diurnal habits. Spectral tuning of cone opsins did not differ among diurnal and nocturnal species. Retinas of nocturnal colubrids had many rows of photoreceptor nuclei, with large numbers of rods, labeled by wheat germ agglutinin (WGA), and two types of cones: large cones sensitive to long/medium wavelengths (L/M) and small cones sensitive to ultra-violet/violet wavelengths (UV/VS). In contrast, retinas of diurnal species had only one row of photoreceptor nuclei, with four types of cones: large and double L/M cones, small UV/VS cones, and a second group of small cones, labeled by WGA.ConclusionsFor LWS gene, selection tests did not confirm different constraints related to activity pattern. For SWS1, stronger purifying selection in nocturnal lineages indicates divergent evolutionary pressures related to the activity pattern, and the importance of the short wavelength sensitivity at low light condition. Activity pattern has a clear influence on the signatures of selection and spectral tuning of RH1, with stronger purifying selection in diurnal lineages, which indicates selective pressure to preserve rhodopsin structure and function in pure-cone retinas. We suggest that the presence of four cone types in primarily diurnal colubrids might be related to the gain of color discrimination capacity.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1110-0) contains supplementary material, which is available to authorized users.

Evolution of the eyes of vipers with and without infrared-sensing pit organs

“…The reason for PNA labelling of all LWS and no SWS1 cones is unclear, PNA being a general cone marker (at least in various mammals, chicken and goldfish; (Blanks & Johnson, 1984)) that attaches to cone-specific components of the interphotoreceptor matrix. PNA labelling of cones has previously been used in colubrid snakes, but that study did not assess whether PNA labelled all cones or only LWS cones (Hauzman et al, 2017).…”

“…Alternatively, the species (and perhaps individuals) are polymorphic. Visual pigment and opsin polymorphism has been reported in several vertebrates (Tan & Li, 1999;Jacobs et al, 2002;Veilleux & Bolnick, 2009), including snakes (Simões et al, 2016b;Hauzman et al, 2017) but its detection is dependent on denser intraspecific sampling than which has typically been carried out to date.…”

The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

“…In comparison to lizards, far less is known about the visual systems of snakes, although in the last few years a plethora of studies have been published (Davies et al, 2009;Hauzman et al, 2014Hauzman et al, , 2017Simões et al, 2015Simões et al, , 2016aSchott et al, 2016;Bhattacharyya et al, 2017;Katti et al, 2018). Snakes in general terms can be separated into Scolecophidia (blindsnakes and wormsnakes), Henophidia (boas, pythons and reatives), and Caenophidia (all other snakes), and in many ways these three groups have distinct visual systems.…”

“…Snakes in general terms can be separated into Scolecophidia (blindsnakes and wormsnakes), Henophidia (boas, pythons and reatives), and Caenophidia (all other snakes), and in many ways these three groups have distinct visual systems. No snake possesses more than three of the possible five opsin classes expressed in reptiles, specifically LWS, SWS1, and RH1 (Davies et al, 2009;Hauzman et al, 2014Hauzman et al, , 2017Simões et al, 2015Simões et al, , 2016aSchott et al, 2016;Bhattacharyya et al, 2017;Katti et al, 2018;Bittencourt et al, 2019;Gower et al, 2019). The first snake visual opsin genes to be sequenced were by Davies et al (2009) in the henophidian royal python (Python regius) and sunbeam snake (Xenopeltis unicolor).…”

“…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").…”