Analysis of the genetically tractable crustacean Parhyale hawaiensis reveals the organisation of a sensory system for low-resolution vision

Abstract

Background Arthropod eyes have diversified during evolution to serve multiple needs, such as finding mates, hunting prey and navigating in complex surroundings under varying light conditions. This diversity is reflected in the optical apparatus, photoreceptors and neural circuits that underpin vision. Yet our ability to genetically manipulate the visual system to investigate its function is largely limited to a single species, the fruit fly Drosophila melanogaster . Here, we describe the visual system of Parhyale hawaiensis , an amphipod crustacean for which we have established tailored genetic tools. Results Adult Parhyale have apposition-type compound eyes made up of ~ 50 ommatidia. Each ommatidium contains four photoreceptor cells with large rhabdomeres (R1–4), expected to be sensitive to the polarisation of light, and one photoreceptor cell with a smaller rhabdomere (R5). The two types of photoreceptors express different opsins, belonging to families with distinct wavelength sensitivities. Using the cis- regulatory regions of opsin genes, we established transgenic reporters expressed in each photoreceptor cell type. Based on these reporters, we show that R1–4 and R5 photoreceptors extend axons to the first optic lobe neuropil, revealing striking differences compared with the photoreceptor projections found in related crustaceans and insects. Investigating visual function, we show that Parhyale have a positive phototactic response and are capable of adapting their eyes to different levels of light intensity. Conclusions We propose that the visual system of Parhyale serves low-resolution visual tasks, such as orientation and navigation, based on broad gradients of light intensity and polarisation. Optic lobe structure and photoreceptor projections point to significant divergence from the typical organisation found in other malacostracan crustaceans and insects, which could be associated with a shift to low-resolution vision. Our study provides the foundation for research in the visual system of this genetically tractable species. Electronic supplementary material The online version of this article (10.1186/s12915-019-0676-y) contains supplementary material, which is available to authorized users.

Light adaptation mechanisms in the eye of the fiddler crab Afruca tangeri

“…Screening pigment granules contract inward to tightly encircle the rhabdom in bright light, then move away from the light path in darkness, functioning as a pupil. Though not widely reported in marine arthropods, it has been observed in the mantis shrimp G. oerstedii (King & Cronin, 1994a, 1994b, a horseshoe crab, Limulus polyphemus (Miller & Cawthon, 1974) and the amphipod Paryhale hawaiensis (Ramos et al, 2019), a diverse mix of arthropod taxa.…”

Evolution of crab eye structures and the utility of ommatidia morphology in resolving phylogeny

“…However, our current knowledge of the genes involved in vision and 820! phototransduction, i.e., the conversion of light to electrochemical signals, is severely limited across decapod crustaceans (Henze and Oakley, 2015;Ramos et al, 2019;Zhang et al, 2019), ! Page -39with all crab data restricted to only a few eubrachyurans.…”

Regionalization in the compound eye ofTalitrus saltator(Crustacea, Amphipoda)

“…Our investigations on T. saltator indicate for the first time in Crustacea the existence of an area located in the DP of its eye specialised in detecting certain wavelength ranges involved in the perception of skylight cues. We still don’t know the role of R5 dominant in DP, however, in Parhyale hawaiensis , the spectral absorption bands estimated from the genetic results differed between R1-4 and R5 (Ramos et al, 2019). Therefore, R5 cell of T. saltator also might have different colour absorption band.…”

“…We assumed that the structural specializations of the retina determines the functional differences between DP and VP, therefore, we estimated roughly the visual filed from the light microscopic data. Since the number of the ommatidia of T. saltator increases with the growth of the body as reported for Parhyale hawaiensis (Ramos et al, 2019) and smaller ommatidial crystalline cones are frequently found at the peripheral region of the eye, we omitted these small ommatidia which possess small crystalline cones when we estimated the visual field. The visual field size in T. saltator were investigated using their pseudopupil (Beugnon et al, 1986); the individuals could potentially detect visual stimuli at 101 ° of vertical elevation.…”