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Molecular evolution and depth-related adaptations of rhodopsin in the adaptive radiation of cichlid fishes in Lake Tanganyika

Citation

Ricci, Virginie; Ronco, Fabrizia; Musilova, Zuzana; Salzburger, Walter (2022), Molecular evolution and depth-related adaptations of rhodopsin in the adaptive radiation of cichlid fishes in Lake Tanganyika, Dryad, Dataset, https://doi.org/10.5061/dryad.4mw6m90c7

Abstract

The visual sensory system is essential for animals to perceive their environment and is thus under strong selection. In aquatic environments, light intensity and spectrum differ primarily along a depth gradient. Rhodopsin (RH1) is the only opsin responsible for dim-light vision in vertebrates and has been shown to evolve in response to the respective light conditions, including along a water depth gradient in fishes. In this study, we examined the diversity and sequence evolution of RH1 in the virtually entire adaptive radiation of cichlid fishes in Lake Tanganyika, focusing on adaptations to the achromatic environment with respect to depth. We show that Tanganyikan cichlid genomes contain a single copy of RH1. The 76 variable amino acid sites detected in RH1 across the radiation were not uniformly distributed along the protein sequence, and 31 of these variable sites show signals of positive selection. Moreover, the amino acid substitutions at 15 positively selected sites appeared to be depth-related, including three key tuning sites that directly mediate shifts in the peak spectral sensitivity, one site involved in protein stability, and 11 sites that may be functionally important on the basis of their physicochemical properties. Among the strongest candidate sites for deep-water adaptations are two known key tuning sites (positions 292 and 299) and three newly identified variable sites (37, 104 and 290). Our study, which is th first compralehensive analysis of RH1 evolution in a massive adaptive radiation of cichlid fishes, provides novel insights into the evolution of RH1 in a freshwater environment.

Methods

For this study, we revisited the Illumina sequence data from our previous work, in which we had produced whole genome sequences for a nearly taxonomically complete sample of the cichlid fish fauna of LT (raw sequencing data are available on NCBI under the BioProject accession number PRJNA550295, https://www.ncbi.nlm.nih.gov/bioproject/Ronco et al., 2021). Making use of the available raw DNA reads, we (i) identified and newly assembled the intron-less RH1 coding sequence; (ii) quantified the diversity of both nucleotides and amino acid sequences of RH1; (iii) tested if environmental pressures have shaped RH1 protein sequence evolution; and (iv) screened for candidate amino acid substitutions that are associated with water depth and hence potentially represent depth-related adaptations.

Usage Notes

A GitHub reposit is available for further information: https://github.com/Ninet93/RH1_Ricci_et_al.git

Funding

European Research Council, Award: 617585

Swiss National Science Foundation, Award: 176039

Swiss National Science Foundation, Award: 166550

Czech Science Foundation, Award: 21-31712S