Visual adaptation of opsin genes to the aquatic environment in sea snakes

Takashi Seiko,Takushi Kishida,Takashi Okitsu,Yohey Terai,Mamoru Toda,Akimori Wada,Takahiko Hariyama,Mina Toyama,Yoko Satta

doi:10.1186/s12862-020-01725-1

Abstract

BackgroundEvolutionary transitions from terrestrial to aquatic life history cause drastic changes in sensory systems. Indeed, the drastic changes in vision have been reported in many aquatic amniotes, convergently. Recently, the opsin genes of the full-aquatic sea snakes have been reported. However, those of the amphibious sea snakes have not been examined in detail.ResultsHere, we investigated opsin genes and visual pigments of sea snakes. We determined the sequences of SWS1, LWS, and RH1 genes from one terrestrial, three amphibious and four fully-aquatic elapids. Amino acid replacements at four and one spectra-tuning positions were found in LWS and RH1, respectively. We measured or predicted absorption of LWS and RH1 pigments with A1-derived retinal. During their evolution, blue shifts of LWS pigments have occurred stepwise in amphibious sea snakes and convergently in both amphibious and fully-aquatic species.ConclusionsBlue shifted LWS pigments may have adapted to deep water or open water environments dominated by blue light. The evolution of opsins differs between marine mammals (cetaceans and pinnipeds) and sea snakes in two fundamental ways: (1) pseudogenization of opsins in marine mammals; and (2) large blue shifts of LWS pigments in sea snakes. It may be possible to explain these two differences at the level of photoreceptor cell composition given that cone and rod cells both exist in mammals whereas only cone cells exist in fully-aquatic sea snakes. We hypothesize that the differences in photoreceptor cell compositions may have differentially affected the evolution of opsins in divergent amniote lineages.

Highlights

Evolutionary transitions from terrestrial to aquatic life history cause drastic changes in sensory systems
Absorption spectra tuning positions in the opsin gene sequences from sea snakes We aligned the amino acid sequences of Short wavelength sensitive opsin 1 (SWS1), Long wavelength sensitive opsin (LWS), and RH1 from 13 species (Additional file 1: Fig. S1, Additional file 2: Table S1), and searched for amino acid replacements that affect the tuning of the absorption spectra of opsin pigments
Among these spectral tuning positions, one amino acid replacement was found at position 292 in RH1 sequences and four replacements were found at positions 164, 181, 269, and 292 in LWS sequences (Fig. 1)

Summary

Introduction

Evolutionary transitions from terrestrial to aquatic life history cause drastic changes in sensory systems. The drastic changes in vision have been reported in many aquatic amniotes, convergently. The opsin genes of the full-aquatic sea snakes have been reported. Those of the amphibious sea snakes have not been examined in detail. Several major extant taxonomic groups have returned to the sea and have adapted to an aquatic environment. Hydrophiin sea snakes have adapted to an aquatic environment. Sea snakes are composed of species in the fully aquatic hydrophiins and amphibious laticaudins ( called sea kraits) [3]. Molecular phylogenetic studies have reported that Hydrophiini forms a monophyletic clade with terrestrial snake species, and this clade forms a sister clade with the amphibious Laticaudini [4, 5]. The divergence time between Hydrophiini and Laticaudini is estimated to be approximately 12–20 million years (Ma) [2, 4, 7]

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