Here, There and Everywhere: The Radiolar Eyes of Fan Worms (Annelida, Sabellidae)

Abstract

Fan worms (Annelida: Sabellidae) possess some of the strangest eyes in nature. Their eponymous fans are composed of two sets of radiolar tentacles that project from the head up out of the worm's protective tube into the water column. Primarily used for respiration and feeding, these radioles are also often involved in photoreception. They display a surprising diversity of eyes of varying levels of sophistication, ranging from scattered single ocelli to compound eyes with up to hundreds of facets. These photoreceptors could represent a relatively recent evolutionary development to cope with a sessile, tube-dwelling lifestyle, and the primary cerebral eyes (haplessly positioned within the tube most of the time) amount to little more than minute pigment cups with scant visual potential. The radiolar eyes on the other hand, appear to function as visual burglar alarms for detecting looming predators and eliciting a startle response for the worm to rapidly retreat within its fortified tube. Despite sometimes resembling arthropod compound eyes, the radiolar photoreceptors have many canonically vertebrate-like physiological characteristics. Considering the unusual and apparently recently evolved nature of the fan worm radiolar photoreceptors, these animals are an excellent case for examining the emergence of novel visual systems, the development of rudimentary visually guided behaviors, and the function of distributed sensory systems. Here, we review over 100 years of investigations into the anatomical diversity of sabellid radiolar photoreceptors and eyes in an evolutionary and functional context. We provide new information on radiolar eye structure in several species of fan worms, and we attempt to organize the various eye types and ocellar structures into meaningful hierarchies. We discuss the developmental, evolutionary, and functional significance of the radiolar eyes and highlight areas of future interest in deciphering their unique nature.

A Go-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii

“…Firstly, developmental data suggest that the anterior appendages of serpulids and sabellids, the radiolar tentacles, are developmentally homologous to Platynereis palpae and not the peristomal cirri [29]. Secondly, the light-sensitive structures of serpulids and sabellids are typically associated with pigment cells [13], which we do not observe in Platynereis (Fig. 2a, f–k).…”

“…3b). This is congruous with research on sabellid worms whose rhabdomeric-type cephalic eyes, likely using rhabdomeric-type opsins, are suggested to play no part in shadow detection due to their occlusion within the animal’s opaque protective tube [13]. …”

“…Such peripheral placement of these photoreceptive structures is likely integral to the reliable detection of shadows, even if they do not pass directly over the cephalic or central region of the animal. The photoreceptive cells in the tentacular structures of both serpulids and sabellids have been thoroughly documented [7, 13], and might appear to be more elaborated versions of the simple cirral Go-opsin1 + photoreceptors in Platynereis dumerilii . However, several differences are apparent.…”

“…The primary function of these photosensitive structures, and those more recently documented in ark clams, is likely to be shadow detection [6], but so far research into the underlying molecular mechanisms of the shadow reflex has been limited due to the dearth of molecular tools available in these model organisms. Platynereis dumerilii, a molecularly slowly evolving [8, 9], morphologically archetypical marine nereidid [10], and distant annelid relative of sabellid fan worms [11–13], with its expansive genetic toolkit [14] and observable, well-characterised shadow reflex [15], represents a useful model to understand the molecular mechanisms and evolution of this behaviour. Platynereis dumerilii is a predominantly nocturnal animal, but the animals also exhibit movement and exploratory behaviour during the day, anchoring their trunks inside protective tubes whilst occasionally reaching out with their heads, likely to survey the environment and to feed [16].…”

Notaulax yamasui sp. n. (Annelida, Sabellidae) from Okinawa and Ogasawara, Japan, with notes on its ecology

“…The fan-worm eyes and other photoreceptors are summarized in Bok and Nilsson (2016) and Bok et al (2016). The compound eyes of Stylomma are stalked, which occurs neither in Megalomma , nor in the swellings of N. yamasui sp.…”