The diversity of opsins in Lake Baikal amphipods (Amphipoda: Gammaridae)

Abstract

Background: Vision is a crucial sense for the evolutionary success of many animal groups. Here we explore the diversity of visual pigments (opsins) in the transcriptomes of amphipods (Crustacea: Amphipoda) and conclude that it is restricted to middle (MWS) and long wavelength-sensitive (LWS) opsins in the overwhelming majority of examined species.

Results: We evidenced (i) parallel loss of MWS opsin expression in multiple species (including two independently evolved lineages from the deep and ancient Lake Baikal) and (ii) LWS opsin amplification (up to five transcripts) in both Baikal lineages. The number of LWS opsins negatively correlated with habitat depth in Baikal amphipods. Some LWS opsins in Baikal amphipods contained MWS-like substitutions, suggesting that they might have undergone spectral tuning.

Conclusions: This repeating two-step evolutionary scenario suggests common triggers, possibly the lack of light during the periods when Baikal was permanently covered with thick ice and its subsequent melting. Overall, this observation demonstrates the possibility of revealing climate history by following the evolutionary changes in protein families.

Keywords: Ancient ecosystems; Crustacea: Malacostraca: Amphipoda; Lake Baikal; Parallel evolution; Vision.

Fig. 1

The diversity of visual opsins in selected representatives of Eumalacostraca and examples of Lake Baikal amphipods. a Visual opsin diversity in selected malacostracan species: Hemisquilla californiensis and Pseudosquilla ciliata (Stomatopoda) [10]; Euphausia superba (Euphausiaceae) [23]; Janicella spinicauda, Systellaspis debilis, Cambarus tenebrosus, Procambarus fallax, and Orconectes incomptus (Decapoda) [11, 12, 24]; Hyalella azteca, Parhyale hawaiensis, Niphargus hrabei, and Gammarus minus (Amphipoda) [14, 16, 25, 26]. In the case of Janicella spinicauda, both photophore and eye opsins were counted. b–g Examples of Lake Baikal amphipods and their ecological characteristics [27]. b Eulimnogammarus maackii (Gersfteldt, 1858), a benthic species mostly found at depths of 0–40 m. c Another benthic species, E. cyaneus (Dybowsky, 1874), mostly concentrating close to the shoreline. d The only pelagic species Macrohectopus branickii (Dybowsky, 1874). e Another littoral benthic species Gmelinoides fasciatus (Stebbing, 1899), a unique species which originated in Baikal but was successfully introduced into multiple water bodies in Siberia and European Russia [28]. f Brandtia latissima latior (Dybowsky, 1874) mostly found at depths from 0.5 to 50 m. g A deep-water eurybathic scavenger Ommatogammarus albinus (Dybowsky, 1874) mainly found below 200 m. Note the presence of large pigmented eyes in the deep-water species

Fig. 2

Multiple losses of MWS opsin expression in Baikal and other amphipods. Species phylogeny (based on one-copy orthologs present in all transcriptomes) is annotated with the number of opsins found. aLRT, approximate likelihood ratio test. aBayes, approximate Bayes test. Talitridae and Gammaridae are marked according to the World Amphipoda Database [66] accessed through the WoRMS database [67]

Fig. 3

Expression levels of LWS and MWS opsins in Gammaridae estimated by the alignment of raw sequencing reads of selected species to the nucleotide sequences of one MWS and two LWS opsins found in the transcriptome of G. pulex. European = European freshwater species (G. pulex, G. fossarum, and G. wautieri). Boxplots are violet-coloured if the median was positive and black-coloured if it was equal to zero. RPM, reads per million

Fig. 4

The results of laboratory experiments in E. cyaneus (a) and Gm. fasciatus (b) show avoidance reactions to different parts of the visible light spectrum. The centres / half widths at half maxima of the spectra of the blue, green, yellow and red LEDs are 457/11, 519/18, 593/8, and 626/8, respectively. Each dot represents the median of one experiment (20 animals). *Stands for p < 0.05 and **stands for p < 0.01 (Mann–Whitney test vs. the control level with Holm’s correction for multiple comparisons)

Fig. 5

The diversity of LWS opsins in Baikal amphipods. a Only the species with at least one opsin detected were analyzed. The two opsins of G. minus are shown for comparison and classification. b The relationship between the number of opsins and habitat depth. The relationship is statistically significant (adjusted ${\text{R}}^2=0.17$; p = 0.003 in a linear model). For more information, see  Additional file 8: Table S5. c Frequent MWS-like substitutions in LWS opsins of Baikal amphipods superimposed on the secondary structure of bovine rhodopsin visualized with Protter [78]. For more information, see Additional file 9: Table S6.