It's the worms' turn

Worms are the earth's custodians. Many ingest and detoxify the ocean's noxious biotic debris, and the Sabellid worms are among the most numerous of these stewards.

Sabellids are polychaete worms found in all the oceans, and are surprisingly common. Coral reefs are rife with them. Almost all Sabellids are filter feeders and, as such, they remove organic refuse or plankton that floats near the bottom or swirls on the currents. The head of sabellids has been transformed into a feathery “crown” comprising radioles that project from a protective tube into the water. This crown filters out the necessary food, but this requires time, meaning long exposure to potential predators. The photograph shows a sabellid (Megalomma sp) with two compound eyes at the end of two of the crown's radioles; these aren't used for feeding but project the furthest away from the worm giving it a wide view.

Each sabellid “eye” consists of 40–60 ommatidia, but these “little eyes” are different, anatomically, from those seen in insects or spiders. The individual ommatidium is a tapered pigmented tube resembling an ice cream cone formed from a single cell with a crystalline core as the “ice cream.” The apex of the cone contains a single photoreceptor that is connected to an axon. The cone‐shaped pigment cell serves to isolate the receptor portion from stray photons and to provide directionality.

Polychaete annelid worms provide a pivotal point for visual mechanisms (BJO cover, January 2005) as some have both invertebrate and vertebrate photoreceptor cell types, but these interesting creatures have other important aspects to their visual mechanisms. The compound eye that so typifies invertebrate vision is almost exclusively restricted to the Arthropoda, but the polychaete worms, along with certain bivalves and a couple of odd stragglers, also have compound eyes. The eyes of the sabellids then represent evolution's separate and disparate attempt at compound eyes, possibly fairly recently, since not all sabellids have them, and certainly none of their close wormy relatives do.

Arthropods, including insects, spiders, and crabs, have exploited compound eyes since the Cambrian explosion (BJO cover, February 2004). Polychaete worms are outliers, though, as their compound eyes have different structural and neurological strategies indicating that the evolutionary process has been actively seeking other ocular designs well after the Cambrian period (Nilsson DE, Phil Trans R Soc Lond B 1994;346:195–212). These different mechanisms offer clues to the early development of photoreception and visual processing as well as the evolution of the photoreceptor.

Photoreceptors are able to absorb light thanks to “visual pigment,” which consists of a protein (called an “opsin”) and a chromophore (that, in vertebrates, is a structural derivative of vitamin A). By inducing structural changes in the visual pigment, photon absorption by the chromophore is able to initiate light responses. The structure and interactions of the chromophore with the opsin determine the peak wavelength that causes the configurational change. To maximise the chance of a response from any single photoreceptor there must be many molecules of photopigment. Since photopigments are membrane bound, the more undulations of the membrane, the more photopigment can be contained in a single cell. Two basic types of cells have developed to contain photopigment with projections, discs, and infoldings—modified microvilli and modified cilia. In general, vertebrates have photopigment contained in modified cilia while those of invertebrates are in cells with modified microvilli. There are enough exceptions to that general rule, however, to suggest that the last common ancestor had both ciliary and microvilli bound photopigment (BJO cover, January 2005).

The sabellids are exceptions to this rule for they are invertebrates that have modified cilia to contain their visual pigment. They also have key neurological differences. When light strikes their photopigment, the configurational change initiates hyperpolarisation of the membrane from a depolarised state, much like the photoreceptors in vertebrates. But in most invertebrates photopigment configurational change initiates depolarisation from a hyperpolarised state. This represents a fundamental difference in ocular development and may be a clue to early photoreception.

The opsins, retinal, and G protein involved in photoreception are truly ancient and may have been available to the first prokaryotic (without a nucleus) cells. Such proteins may have functioned in early prokaryotes as proton pumps and, hence, energy sources. When cellular or metazoan predation began, however, these proteins probably could serve the cell, or cells, in other ways. These proteins could verify a change in light levels especially with shadows. If the membrane began to be hyperpolarised, and a shadow represented a threat, evolution would have selected the model that depolarised with a shadow or darkness as a protective mechanism in prey species. If the membrane containing the photopigment depolarised with shadows or darkness in prey species, then hyperpolarisation would be induced with a light stimulus.

The compound eyes found in most arthropods generally initiate the signalling with depolarisation of the photoreceptor membrane from a hyperpolarised state. Perhaps this would reflect an initial a predatory lifestyle instead of a defensive one because the predator would be stimulated by light, not shadows or darkness. Since extant arthropods are probably descended from the predatorial species of the Cambrian period, the vertebrates may well be descended from the lowly worms. I guess it is just the worms' turn.