Cerebral photoreception in mantis shrimp

Abstract

The currently unsurpassed diversity of photoreceptors found in the eyes of stomatopods, or mantis shrimps, is achieved through a variety of opsin-based visual pigments and optical filters. However, the presence of extraocular photoreceptors in these crustaceans is undescribed. Opsins have been found in extraocular tissues across animal taxa, but their functions are often unknown. Here, we show that the mantis shrimp Neogonodactylus oerstedii has functional cerebral photoreceptors, which expands the suite of mechanisms by which mantis shrimp sense light. Illumination of extraocular photoreceptors elicits behaviors akin to common arthropod escape responses, which persist in blinded individuals. The anterior central nervous system, which is illuminated when a mantis shrimp's cephalothorax protrudes from its burrow to search for predators, prey, or mates, appears to be photosensitive and to feature two types of opsin-based, potentially histaminergic photoreceptors. A pigmented ventral eye that may be capable of color discrimination extends from the cerebral ganglion, or brain, against the transparent outer carapace, and exhibits a rapid electrical response when illuminated. Additionally, opsins and histamine are expressed in several locations of the eyestalks and cerebral ganglion, where any photoresponses could contribute to shelter-seeking behaviors and other functions.

Figure 1

The pigmented ventral eye and the cerebral ganglion (CG), or brain, of Neogonodactylus oerstedii. (A) The CG is housed within the cephalothorax behind the eyes (oval). (B) A ventral view of an illuminated cephalothorax reveals a slightly darker region (arrow) that corresponds to the ventral eye location on the surface of the isolated CG. (C) A prominent pigmented structure (arrow) is visible toward the anterior end on the ventral surface of an isolated CG of adult N. oerstedii. The ventral eye we identified in an adult mantis shrimp is similar in location to the ventral eye in mantis shrimp larvae.

Figure 2

Behavioral evidence for extraocular photoreception in mantis shrimp. Whole-body illumination elicits common escape responses (tail-flipping, walking, and swimming) in normal and blinded mantis shrimp. These behaviors were observed less frequently when mantis shrimp are left in the dark without burrows. *P < 0.05; **P < 0.01.

Figure 3

Electrophysiological evidence for extraocular photoreception in mantis shrimp. Illumination of the eyeless mantis shrimp cephalothorax produced electrical responses in AC recordings from the ventral eye. Shown are data for three preparations that varied in response magnitude upon stimulation with the same 0.5 s white light flash (6.14 × 10¹⁵ photons cm² s¹). The onset of light stimulation is indicated by the “on” phase of the positive square wave. Black lines are mean ERG response (n = 2−5 light flashes per preparation), grey shading is standard deviation.

Figure 4

Opsin transcripts are expressed in the anterior portion of the central nervous system of Neogonodactylus oerstedii. In situ hybridization labeling patterns of 60 μm sagittal optic lobe sections (left column) and transverse cerebral ganglion (CG) sections (right column) show that of the four opsin transcripts expressed in the CG, only two are expressed within the retina and/or neural tissue within the eyestalk carapace. NoMWS1 is expressed in cell bodies surrounding several neuropils—the lamina (La), medulla (M), lobula (Lo), and hemiellipsoid body (HB)—within the eyestalk, and may be expressed in the most dorsal photoreceptors in the retina. NoLWS1 riboprobe labels the dorsal hemisphere (DH) and ventral hemisphere (VH) of the retina, but not the equatorial midband (MB) rows. Within the CG, NoMWS1 and NoLWS3 are expressed in the ventral eye (VE, arrows), which lies anterior to the central complex (CX). NoLWS1 and NoLWS2 are expressed in several regions with densely-packed, large cell bodies (arrowheads) that surround the antennal neuropil (AnN), olfactory lobe (OL), lateral antennular neuropil (LAN), and olfactory-glomeruli tract (OGT). An anatomical diagram summarizes NoMWS1 (teal), NoLWS1 (dark blue), NoLWS2 (green), and NoLWS3 (purple) transcript expression in the optic lobes and CG.

Figure 5

Labeling patterns of antibodies designed to characterize opsin protein (magenta) and histamine (white) expression are consistent with in situ labeling of opsin transcripts. Cytoskeletal tubulin and cell nuclei are visualized using anti α-tubulin antibody (green) and DAPI (cyan), respectively. (A) A coronal retinal section shows that antibody designed against crayfish long-wavelength-sensitive opsin labels all photoreceptors in the mantis shrimp (Neogonodactylus oerstedii) retina. (B) A sagittal view of the optic lobe shows that anti-opsin antibody labels the hemiellipsoid body (HB) and protocerebrum (P). (C) A sagittal section of the optic lobe shows that anti-histamine antibody labels tissue throughout the optic lobe, including the protocerebrum. (D) A transverse section of the cerebral ganglion (CG) reveals anti-opsin antibody labeling of the ventral eye (arrow), dense clusters of cell bodies (arrowheads), and periphery of the olfactory lobes (OL). (E) The ventral eye (arrow) is visualized in a transverse CG section and appears to extend large neuronal bundles to posterior brain regions (asterisks). The anti-opsin antibody also labels cell bodies around the periphery of the CG (arrowheads). (F) Anti-histamine antibody labeling is consistent with anti-opsin antibody labeling throughout the transverse CG section, including the VE (arrow, inset in F). Lobula (Lo); medulla (M).