Multiple spectral channels in branchiopods. I. Vision in dim light and neural correlates

Abstract

Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda+Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here, we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and the optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral freshwater habitats.

Multiple spectral channels in branchiopods. II. Role in light-dependent behavior and natural light environments

“…We have found that ephemeral pool habitats, at less than 1 m of depth, are often dimmer than terrestrial habitats under starlight. In a companion article (Lessios et al, 2018), we found that branchiopod apposition compound eyes are likely to generate reliable signals at such intensities. There is some neuroanatomical evidence that pancrustaceans might incorporate summation from compound eye ommatidia in the lamina of their optic lobes for reliable vision at low intensities (Glantz, 2014;O'Carroll and Warrant, 2017;Warrant, 2017).…”

“…There is also evidence that recently duplicated paralogs are maintained at a much higher rate than would be expected given homogenization by gene conversion (Colbourne et al, 2011). In a companion paper (Lessios et al, 2018), we suggest that branchiopods have maintained four spectral classes of photoreceptors in their compound eyes, which is supported by the number of opsins expressed in anostracan and notostracan compound eyes (Kashiyama et al, 2009). Based on the number of spectral photoreceptor classes alone, it might be assumed that these species possess tetrachromatic vision.…”

“…In T. longicaudatus, summation of outputs from multiple spectral classes could take place from broad receptive fields present in the lamina that we have identified in a companion paper (Lessios et al, 2018). The narrow bandwidth of photopositive responses we found for male S. mackini strongly supports the use, and the presence, of a single spectral photoreceptor class with an absorptance peak near 532 nm identified in a companion paper (Lessios et al, 2018). There are several possibilities regarding how a single receptor could provide input for narrow-bandwidth photopositive behavior.…”

“…The structural properties of the visual neuropils that have been identified in branchiopods to date, which do not include a medulla or a lobula, therefore suggest a lesser ability to process color information. In a companion paper, we have clarified how the structure of the lamina, the first optic neuropil, is configured (Lessios et al, 2018). Here, we hypothesize that light attenuation and the spectral content available in ephemeral pools act as a selective pressure for light-dependent behavior that is determined by a simplified set of optic neuropils.…”

“…Despite having only two neuropils in their optic lobes, all branchiopods studied to date express four or more rhabdomeric opsins in their compound eyes (Kashiyama et al, 2009). In a companion paper (Lessios et al, 2018), we report that these opsins are most likely configured in four spectral photoreceptor classes in their compound eyes, which agrees with electroretinography of branchiopods studied to date, and the most recent rhabdomeric opsin phylogeny of pancrustacean compound eyes (Henze and Oakley, 2015;Smith and Macagno, 1990). In the first optic neuropil, the lamina, we identified lateral processes as neuroanatomical candidates for spatial summation in dim light conditions.…”