Expression of opsins, ultrastructure of eyes, and light-induced behaviour in tardigrades (water bears): Insights into the evolution of visual systems and photoreception in panarthropods
Systematics and Morphology (Zoology)
Final Report Abstract
Numerous gaps existed in our knowledge with regard to the expression patterns of opsins, the ultrastructure of the eye, and light-induced behavior in tardigrades (water bears). The present project set out to close these gaps and to provide insights into the evolution of visual systems and photoreception in panarthropods (tardigrades + onychophorans + arthropods). Despite various obstacles, all major goals of the project have been achieved, the majority of initial questions have been clarified, and several exciting discoveries have been made. The ultrastructural data confirm that the eye of the tardigrade Hypsibius exemplaris contains both rhabdomeric and ciliary receptor cells, but only the rhabdomeric cell seems to be responsible for directional photoreception. Prominent expression of a rhabdomeric opsin (R-opsin-1) is associated with this cell and occurs in the bundle of microvilli located within the groove of the pigment cell. The only other opsin localized within the eye of H. exemplaris is C- opsin-1, which is closely associated with the highly modified cilium (labyrinth) of the ciliary cell. The C-opsin-1 immunoreactivity within this region suggests that the labyrinth may serve to increase surface area, thereby enhancing the sensitivity of the ciliary receptor cell to external stimuli. Its position outside the pigment cell indicates that it is not involved in directional photoreception. The simple structure of the tardigrade eye suggests that its visual properties are very limited, as this organ is most likely able to resolve only one pixel. We have further detected Cytotardin, a cytoplasmic lamin, in ocular cells, which is otherwise only found in the epidermis and epithelial linings of the fore- and hindgut. Thus, Cytotardin associated with the cell-cell junctions and stabilizing the different components of the eye points to an epidermal origin of the tardigrade eye. Our discovery of widespread, tissue-specific expression of nine opsins in almost every major organ of H. exemplaris suggests that these proteins play a role in many different processes. While the function of the r-opsin in the rhabdomeric cell of the eye is clear, the functions of the remaining eight opsins can only be speculated upon based on the known morphology and/or postulated function of the respective structures where they are localized. One of the most exciting discoveries we made is the evidence of the so-called intergenic trans-splicing of the two neuropsin genes in H. exemplaris, which results in a vast diversity of splice variants and exon combinations between these two genes. The role of this mechanism is unknown, but it might promote functional diversification of neuropsins, while at the same time not affecting the size of the tardigrade genome. Finally, our data on light-induced behavior and spectral sensitivity in H. exemplaris revealed that specimens of this species exhibit positively phototactic behavior towards white light and respond strongest to blue and green light between 470 nm and 520 nm. The photopositive reaction in H. exemplaris matches observations in other eutardigrades, which might be related to their typical limnic/limnoterrestrial habitats and nutrition on green algae. In contrast to previous results in a Macrobiotus species, our findings did not reveal photokinetic or photophobic behavior in H. exemplaris. The experimental setup established in the present study can increase the reproducibility of results and might prove useful for comparing light-induced behavior across tardigrade species from different habitats, thus complementing our knowledge about this elusive group of animals.
Publications
- (2017): The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 203: 565–590
Martin, C., Gross, V., Hering, L., Tepper, B., Jahn, H., Oliveira, I.S., Stevenson, P.A. & Mayer, G.
(See online at https://doi.org/10.1007/s00359-017-1186-4) - (2019): Miniaturization of tardigrades (water bears): Morphological and genomic perspectives. Arthropod Structure and Development 48: 12–19
Gross, V., Treffkorn, S., Reichelt, J., Epple, L., Lüter, C. & Mayer, G.
(See online at https://doi.org/10.1016/j.asd.2018.11.006) - (2021): Organization of the central nervous system and innervation of cephalic sensory structures in the water bear Echiniscus testudo (Tardigrada: Heterotardigrada) revisited. Journal of Morphology 282: 1298–1312
Gross, V., Epple, L. & Mayer, G.
(See online at https://doi.org/10.1002/jmor.21386)
