Unique photoreceptor arrangements in a fish with polarized light discrimination

Abstract

In contrast to other vertebrates, some anchovies have cone photoreceptors with longitudinally oriented outer segment lamellae. These photoreceptors are axially dichroic (i.e., they are sensitive to the polarization of axially incident light) and form the basis of a polarization detection system in the northern anchovy, Engraulis mordax. Whether other cone types exist in the retina of this animal, and whether multiple cone opsins are expressed in the retinas of anchovies, is unknown. Likewise, a detailed examination of photoreceptor ultrastructure in nondichroic photoreceptors has not been carried out despite its importance to understand visual specializations within the retina and its use in the formulation of models to explain cellular structure. Here, I combined light and electron microscopy with immunohistochemical studies of opsin expression to infer mechanisms of lamellar formation and to evaluate the potential for color vision in the northern anchovy retina. Morphological observations revealed three cone formations: 1) continuous rows made up of alternating long and short (bilobed) cones with longitudinally oriented lamellae that are orthogonal between cone types; 2) continuous rows of alternating long and short cones in which only the short cones have longitudinally oriented lamellae; and 3) rows of triple cones with transversely oriented lamellae, each triple cone consisting of two lateral cones flanking a small central cone. Ultrastructure investigations supported two models of outer segment formation resulting in the longitudinally oriented lamellae of long and short cones. In the case of the long cone, lateral compression of the outer segment, potentially via the formation of guanine platelet stacks in neighboring pigment epithelium cells, results in a shape transformation from conical to cunate and a tilt from transverse to longitudinal lamellae. In the case of the short (bilobed) cone, membrane invaginations from the connecting ciliary structure grow longitudinally to form a dichroic stack. Opsin expression studies indicated that all cones express middle-to-long wavelength opsins, with long and lateral cones possessing a different opsin from that in short and central cones, confirming the potential for color vision. Together with the ultrastructural observations, these results suggest that the unique cone topography in the northern anchovy retina may underlie a visual system with segregated color and polarization detection channels.

Three cone opsin genes determine the properties of the visual spectra in the Japanese anchovy Engraulis japonicus (Engraulidae, Teleostei)

“…The results of the immunochemical labeling of the photoreceptors of closely related species, specifically the northern anchovy Engraulis mordax by RH1 and LWS antibodies (Novales Flamarique, 2011), are in accordance with our conclusions about the opsin content in the lateral components of the triple and long cones, as well as the opsin difference between the central component of triple cones and that of the long and lateral cones. The somewhat confusing labeling results (i.e.…”

“…Considering that the distribution map of different cones across the retina is not uniform (Koch et al, 2010;Novales Flamarique, 2011;Zueva and Govardovskii, 1991) and given our MSP results, a pattern for the gene expression in cones can be outlined. In the central component of the triple cones the short-wave subclass of the RH2 gene is expressed; furthermore, in both lateral components of the triple cones a combination of the long-wave subclass of RH2 and the LWS genes are expressed.…”

“…The planes of the lamellae of the long and short cones run parallel to the cell axis in the most retinal areas and the lamellar planes of both types of cones are orthogonal to each other, providing a structural basis for detection of polarized incidental light (Awaiwanont et al, 2001;Fineran and Nichol, 1978;Novales Flamarique and Hárosi, 2002;Novales Flamarique, 2011;Novales Flamarique and Hawryshyn, 1998;Zueva, 1981). The triple cones, potentially involved in color vision, apparently lack polarization sensitivity because their lamellae in the outer segments are in a normal transverse position relative to the cell axis (Zueva and Govardovskii, 1991;Hess, 2009;Novales Flamarique, 2011). Thus, anchovies possess color and polarization vision in the same retina, and these two forms of vision are enabled by different combinations of visual pigments.…”

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

“…After 24h fixation at 4°C, the retina was extracted from the eyecup, rinsed in 0.08moll -1 phosphate buffer, and pieces cut using the same procedure as for in situ hybridization. These pieces were processed for embedding in EPON resin blocks, which were cut radially in 75nm steps, as detailed previously (Novales Flamarique, 2011), to reveal the overall morphology and the ultrastructure of cones. Electron micrographs were used to obtain average dimensions of cone outer segments and lamellae, and lamellar spacing.…”

Circular polarization vision in stomatopod crustaceans

“…Many animals are sensitive to LPL, especially invertebrates such as insects and crustaceans (Duelli and Wehner, 1973, Rossel and Wehner, 1984, Marshall, 1988, Schwind, 1991, but also some vertebrates including fish, birds and amphibians (Adler and Taylor, 1973, Able, 1982, Hawryshyn, 1992, Deutschlander and Phillips, 1995, Hawryshyn, 2000, Muheim et al, 2007, Novales Flamarique, 2011. The anatomical requirements and function of the polarization vision system in invertebrates is well researched and understood.…”