Is the Schwabe organ a retained larval eye? Anatomical and behavioural studies of a novel sense organ in adult leptochiton asellus (Mollusca, Polyplacophora) indicate links to larval photoreceptors

The discovery of a sensory organ, the Schwabe organ, was recently reported as a unifying feature of chitons in the order Lepidopleurida. It is a patch of pigmented tissue located on the roof of the pallial cavity, beneath the velum on either side of the mouth. The epithelium is densely innervated and contains two types of potential sensory cells. As the function of the Schwabe organ remains unknown, we have taken a cross-disciplinary approach, using anatomical, histological and behavioural techniques to understand it. In general, the pigmentation that characterises this sensory structure gradually fades after death; however, one particular concentrated pigment dot persists. This dot is positionally homologous to the larval eye in chiton trochophores, found in the same neuroanatomical location, and furthermore the metamorphic migration of the larval eye is ventral in species known to possess Schwabe organs. Here we report the presence of a discrete subsurface epithelial structure in the region of the Schwabe organ in Leptochiton asellus that histologically resembles the chiton larval eye. Behavioural experiments demonstrate that Leptochiton asellus with intact Schwabe organs actively avoid an upwelling light source, while Leptochiton asellus with surgically ablated Schwabe organs and a control species lacking the organ (members of the other extant order, Chitonida) do not (Kruskal-Wallis, H = 24.82, df = 3, p < 0.0001). We propose that the Schwabe organ represents the adult expression of the chiton larval eye, being retained and elaborated in adult lepidopleurans

Anatomy and ultrastructure of the adult larval eye within the chiton Schwabe organ.

<p>A, Semi-thin section showing pigmented epithelium and secondary pigmented structure (chevron) in the Schwabe organ in <i>Leptochiton asellus</i>; the pallial cavity is to the right as shown. lnc, lateral nerve cord; m, mouth; ner, nerve. Scale bar, 100 μm. B, Semi-thin section showing epithelial and secondary pigmented structures observed the region of the Schwabe organ. Scale bar, 50 μm. C, Ultrastructure of the larval eye (from Fischer, 1980). Scale bar, 2 μm. D, Ultrastructure of the pigmented subepithelial structure. Insets from main image; i, putative ciliary roots (chevron); ii, nerve bundles; iii, membrane folding (chevron). lu, lumen; me, mesoderm; mt, mitochondrion; ner, nerve; p, pigment; pb, large pale bodies; asterisk, elongated dark structure. Scale bar, 10 μm.</p

Behavioural experiments to test response of the Schwabe organ to upwelling light.

<p>Percentage of time spent in the darkened quadrants by the four subject groups. S indicates innate presence of Schwabe organ (<i>Leptochiton asellus</i>), X indicates innate absence of Schwabe organ (<i>Lepidochitona cinerea</i>); + indicates subject intact,–indicates ablation surgery. Error bars indicate standard error and are intended as visual guidelines only. Letter codes above bars denote statistically equivalent time spent in the darkened quadrants between treatment groups (based on KW post hoc pairwise comparisons).</p

The Schwabe organ in <i>Leptochiton asellus</i> and the larval eye.

<p>A, Schwabe organ in a fresh glutaraldehyde-fixed specimen. B, Several months after death. Note the persistence of a concentrated dot at the anterior edge (chevron). Scale bar, 500 μm. C, The larval eye in <i>Lepidochitona cinerea in ovo</i> (chevron). Scale bar, 200 μm. D, The ventral migration of the larval eye of <i>Leptochiton asellus</i>. Left to right; dorsal view of developing trochophore with visible shell fields; lateral view with larval eye visible; ventral view with larval eyes having migrated to position lateral to the tip of the foot; metamorphosed larva with larval eyes in final position, reminiscent of the Schwabe organ. Adapted from Christiansen, 1954. E, The position of the larval eye in the anterior nervous system of <i>Lepidozona mertensii</i> (purple, adapted from Heath, 1904). Buccal ganglia and nerves are highlighted in green. Scale bar, 1 mm. F, The position of the Schwabe organ in the anterior nervous system of adult <i>Leptochiton asellus</i>. Scale bar, 1 mm. ac, anterior commissure; bg, buccal ganglia (in green); srg, subradular ganglia.</p

A new sensory organ in "primitive" molluscs (Polyplacophora Lepidopleurida), and its context in the nervous system of chitons

Introduction: Chitons (Polyplacophora) are molluscs considered to have a simple nervous system without cephalisation. The position of the class within Mollusca is the topic of extensive debate and neuroanatomical characters can provide new sources of phylogenetic data as well as insights into the fundamental biology of the organisms. We report a new discrete anterior sensory structure in chitons, occurring throughout Lepidopleurida, the order of living chitons that retains plesiomorphic characteristics. Results: The novel "Schwabe organ" is clearly visible on living animals as a pair of streaks of brown or purplish pigment on the roof of the pallial cavity, lateral to or partly covered by the mouth lappets. We describe the histology and ultrastructure of the anterior nervous system, including the Schwabe organ, in two lepidopleuran chitons using light and electron microscopy. The oesophageal nerve ring is greatly enlarged and displays ganglionic structure, with the neuropil surrounded by neural somata. The Schwabe organ is innervated by the lateral nerve cord, and dense bundles of nerve fibres running through the Schwabe organ epithelium are frequently surrounded by the pigment granules which characterise the organ. Basal cells projecting to the epithelial surface and cells bearing a large number of ciliary structures may be indicative of sensory function. The Schwabe organ is present in all genera within Lepidopleurida (and absent throughout Chitonida) and represents a novel anatomical synapomorphy of the clade. Conclusions: The Schwabe organ is a pigmented sensory organ, found on the ventral surface of deep-sea and shallow water chitons; although its anatomy is well understood, its function remains unknown. The anterior commissure of the chiton oesophagial nerve ring can be considered a brain. Our thorough review of the chiton central nervous system, and particularly the sensory organs of the pallial cavity, provides a context to interpret neuroanatomical homology and assess this new sense organ

Do chitons have a compass? Evidence for magnetic sensitivity in Polyplacophora

Sumner-Rooney, Lauren H., Murray, James A., Cain, Shaun D., Sigwart, Julia D. (2014): Do chitons have a compass? Evidence for magnetic sensitivity in Polyplacophora. Journal of Natural History 48 (45-48): 3033-3045, DOI: 10.1080/00222933.2014.959574, URL: http://dx.doi.org/10.1080/00222933.2014.95957